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R. F. Chapman
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Published in the United States of America by Cambridge University Press, New York
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Preface xi
Acknowledgments xiii
1 Head 3
1.1 Head 3
1.2 Neck 6
1.3 Antennae 8
References 11
4 Nutrition 69
4.1 Nutritional requirements 69
4.2 Balance of nutrients 78
4.3 Feeding on nutritionally poor substrates 82
4.4 Nutritional effects on growth and development 89
References 91
[v]
vi CONTENTS
10 Muscles 229
10.1 Structure 229
10.2 Changes during development 239
10.3 Muscle contraction 244
10.4 Energetics of muscle contraction 249
10.5 Muscular control in the intact insect 251
References 253
PART V Communication
A. Physiological Co-ordination Within the Insect
22 Vision 587
22.1 Compound eyes 587
22.2 Functioning of the eye 592
22.3 Vision 600
22.4 Dorsal ocelli 603
22.5 Stemmata 605
22.6 Other visual receptors 606
References 607
23 Mechanoreception 610
23.1 Cuticular mechanoreceptors 610
23.2 Chordotonal organs 617
23.3 Stretch receptors 629
References 633
24 Chemoreception 636
24.1 Olfaction 636
24.2 Contact chemoreception 645
References 652
The 30 years since the first appearance of this book have the breadth of interest in insects is, perhaps, greater than
seen a revolution in biology and the impact on entomology anywhere else in the world. Through the Center for Insect
has been enormous. In writing the first edition, I tried to Science, I have encountered an extraordinarily diverse
approach the insect as a whole organism and to combine array of scientists working with insects. This has greatly
functional morphology with physiology. That is still my broadened my knowledge of many aspects of insect
aim in this rewriting, but the growth of biological science biology and, I believe, has contributed greatly to my ability
has required me continually to make decisions about where to undertake this revision.
to draw the line. In particular, I felt it was impossible for Throughout the several years that rewriting has
me to do justice to molecular studies. I made this decision taken, I have had constant support from my colleagues in
reluctantly, because molecular biology is so obviously a key the Division of Neurobiology at the University of
to our understanding of how insects work, and I do make Arizona. I thank them for their understanding and help.
some reference to molecular work, especially where it Various colleagues have also made significant contribu-
causes us to rethink older ideas. tions to specific chapters. They are: the late Ed Arbas,
I believe it is critically important to produce a synthesis Norm Davis, John Glendinning, Rick Levine, David
in a single volume. This is essential for the students of Morton and Leslie Tolbert of the Division of
entomology for whom the book was, and is, primarily Neurobiology, Henry Hagedorn of the Department of
intended. I hope, also, to provide a useful reference for Entomology, J.E. Baker, of the USDA, Savannah, USA,
biologists in other fields who use insects as models, but I and Robin Wootton, of the University of Exeter, UK.
want to encourage them to think of the insect as a whole. Many colleagues around the world have graciously
Where does their system belong in the functioning of the allowed me to see preprints of their papers and have con-
organism? Systems in isolation sometimes don’t make tributed in countless other ways. I am grateful to them all.
much sense. I hope they will forgive me for not referring to them all
While I have retained the major divisions that I used in individually.
the earlier editions, I have combined some chapters and In this edition I have included a few photographs and I
rearranged them to some extent. I have adopted American appreciate the willingness with which my scientific col-
spellings throughout. This was done, not without misgiv- leagues have provided them, often going to great lengths to
ings, but the principal market for the book is in North fill my requests. They are: Dr E.A. Bernays, Dr R. Dallai,
America, and the United States is my home. Nevertheless, Dr A.R. Fontaine, Dr A.P. Gupta, Dr S.G.S. Gunnarson,
I confess that ‘esophagus’ does stick in the gullet! Dr B.G.M. Jamieson, Dr J.H. Koenig, Dr M. Locke,
To facilitate further study, I have cited reviews wher- Dr I.A. Meinertzhagen, Dr A.F. Rowley, Dr D.S. Smith,
ever a recent review was known to me and I have consider- Dr R.A. Steinbrecht, Dr F. Tjallingii, and Dr L.T.
ably extended the references to primary literature. In Wasserthal. Chip Hedgecock has been an ever-willing
doing this, I have tried to select recent papers, even though helper in the preparation of these photographs for publi-
these may not always be the most relevant. My aim is to cation.
give an entrée to the literature, rather than to cite a particu- Throughout I have been supported by Elizabeth
lar paper. In an attempt to standardize the names of taxa, I Bernays. She has read and re-read every word, checked
have followed the terminology used in the 1991 edition of every illustration and made innumerable suggestions to
The Insects of Australia. improve the content and presentation. She has also kept
I have been extremely fortunate, and privileged, to have me fed and watered! Without her love I could never have
spent the last few years at the University of Arizona where completed the task.
[xi]
xii PREFACE
Tracey Sanderson at Cambridge University Press has Sonderegger and Ron Adams, and the University of
also been an unfailing support. She, too, has been through Arizona’s Authors’ Support Fund helped defray some of
the whole manuscript with a fine tooth comb. Her com- the costs. Terry Villelas painstakingly typed most of the
ments on the manuscript have done much to make it more tables.
readable. I also appreciate her helpful and timely feedback
to my many questions. Reg Chapman Tucson, Arizona
Some of the illustrations were done by Kristin July, 1997
Acknowledgments
The following publishers and societies have kindly allowed me to Fig. 21.4b. Reprinted from General and Comparative
use illustrations from previously published work: Endocrinology, W.S. Herman & L.I. Gilbert. The
neuroendocrine system of Hyalophora, pp. 275–91, 1966, by
Academic Press Ltd permission of the publisher Academic Press Limited Orlando.
Fig. 2.13a. Reprinted from Animal Behaviour, 34, S.J. Simpson & Fig. 21.10a. Reprinted from Advances in Insect Physiology, 18,
R.J. Ludlow, Why locusts start to feed, pp. 480–96, 1986, by S.S. Tobe & B. Stay, Structure and regulation of the corpus
permission of the publisher Academic Press Limited London. allatum, pp. 305–432, 1985, by permission of the publisher
Fig. 3.26a. Reprinted from Advances in Insect Physiology, 19, Academic Press Limited London.
J.E. Phillips, J. Hanrahan, M. Chamberlain & B. Thomson, Fig. 26.12. Reprinted from Animal Behaviour, 29, D.E. Cowling
Mechanism and control of reabsorption in the insect hindgut, & B. Burnet, Courtship songs and genetic control of their
pp. 329–422, 1986, by permission of the publisher Academic acoustic characteristics in sibling species of the Drosophila
Press Limited. melanogaster subgroup, pp. 924–35, 1981, by permission of
Fig. 5.27d. Reprinted from Journal of Ultrastructure Research, 64, the publisher Academic Press Limited London.
M. Monpeyssin & J. Baeulaton, Hemocytopoiesis in the oak Fig. 26.20b. Reprinted from Biological Journal of the Linnean
silkworm, pp. 35–45, 1978, by permission of the publisher Society, 24, M.F. Claridge, J. den Hollander & J.C. Morgan,
Academic Press Limited Orlando. Variation in courtship signals and hybridization between
Fig. 10.1e,f. Reprinted from Muscle, D.S. Smith, 1972, by geographically definable populations of the rice brown
permission of the publisher Academic Press Limited Orlando. planthopper, Nilaparvata, pp. 35–49, 1985, by permission of
Fig. 10.7. Reprinted from Advances in Insect Physiology, 1, D.S. the publisher Academic Press Limited London.
Smith & J.E. Treherne, Functional aspects of the organization Fig. 27.20a. Reprinted from Advances in Insect Physiology, 14,
of the insect nervous system, pp. 401–84, 1963, by permission B.W. Staddon, The scent glands of Heteroptera, pp. 351–418,
of the publisher Academic Press Limited London. 1979, by permission of the publisher Academic Press Limited
Fig. 12.18a. Reprinted from Advances in Insect Physiology, 24, London.
D.W. Stanley-Samuelson, Prostaglandins and related
eicosanoids in insects, pp. 115–212, 1994, by permission of the Addison Wesley Longman Ltd
publisher Academic Press Limited London. Fig. 15.41
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Mazur, J.C. Regier, F.C. Kafatos, The silkmoth chorion: American Association for the Advancement of Science
morphogenesis of surface structures, pp. 305–21, 1980, by Fig. 10.20 reprinted with permission from Science, 268, 50–1.
permission of the publisher Academic Press Limited Orlando. Copyright 1995 American Association from the Advancement
Fig. 15.20a. Reprinted from Developmental Biology, 26, G. of Science.
Schubiger, Regeneration, duplication and transdetermination
in fragments of the leg disc of Drosophila, pp. 277–95, 1971, American Institute of Physics
by permission of the publisher Academic Press Limited Fig. 23.18a
Orlando.
Fig. 17.15. Reprinted from Advances in Insect Physiology, 26, L.T. American Physiological Society
Wasserthal, Interaction of circulation and tracheal ventilation Figs. 8.19, 8.27c
in holometabolous insects, pp. 297–351, 1996, by permission of
the publisher Academic Press Limited London. Annual Reviews Inc.
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H. Komnick, Chloride cells and chloride epithelia of aquatic volume 37, copyright 1992, by Annual Reviews Inc.
insects, pp. 285–329, 1977, by permission of the publisher Fig. 19.17c with permission from the Annual Review of
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[xiii]
xiv ACKNOWLEDGMENTS
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volume 38, copyright 1985, by Annual Reviews Inc. Schmitz & H. Komnick, Rectale Chloridepithelium und
osmoregulatorische salzaufnaume durch den Enddarm von
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Fig. 12.4a Fig. 3.22. Reprinted from Journal of Insect Physiology, 10,
W.A.L. Evans & D.W. Payne, Carbohydrases in the alimentary
Biological Bulletin of the Marine Biological Laboratory, tract of the desert locust, pp. 657–74, 1964.
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Pharmacology, 1985, vol. 4, pp. 313–90.
Blackwell Scientific Publications Ltd Fig. 4.7b. Reprinted from the Journal of Insect Physiology, 28,
Figs. 2.8, 2.12a, 4.11, 4.12. 13.8b, 13.10, 15.2b, 24.4, 24.9b M.E. Montgomery, Life-cycle nitrogen budget for the gypsy
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Fig. 4.10. Reprinted from the Journal of Insect Physiology, 38,
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W.A. Prosser, S.J. Simpson & A.E. Douglas. How an aphid
Figs. 10.21, 12.4b
symbiosis responds to variation in dietary nitrogen, pp. 301–7,
1992.
Chapman & Hall
Fig. 4.14 Reprinted from Comparative Biochemistry and
Figs. 2.6a,b, 2.7a, 2.13b
Physiology, 98A, M.G. Kaufman & P.A. Klug, The
contribution of hindgut bacteria to dietary carbohydrate
Churchill Livingstone
utilization by crickets, pp. 117–23, 1992.
Figs. 2.16b, 2.17, 3.7a, 3.8a, 3.12b, 6.3a–c, 6.6, 24.2b
Fig. 4.15. Reprinted from the Journal of Insect Physiology, 33,
A.E. Douglas & A.F.G. Dixon, The mycetocyte symbiosis of
Cold Spring Harbor Laboratory Press aphids, pp. 109–13, 1987.
Figs. 15.20b–d, 15.21b,c Fig. 4.16b. Reprinted from the Journal of Insect Physiology, 38,
W.A. Prosser & A.E. Douglas, A test of the hypothesis that
Company of Biologists Ltd nitrogen is upgraded and recycled in an aphid symbiosis, pp.
Figs. 2.9, 2.10b,d, 3.8b, 3.24, 4.13, 5.13, 8.16, 8.18, 9.20, 9.24, 93–9, 1992.
9.25, 9.27, 9.28, 9.34b,c, 9.37, 10.4, 10.9, 13.19a,c, 15.19b, Fig. 5.6a–c. Reprinted from the International Journal of Insect
16.23a, 17.19, 18.6, 18.11a, 18.14a, 19.1a, 19.2b, 19.3a,b, Morphology & Embryology, 22, H.W. Krenn & G. Pass, Wing
19.8, 19.9, 19.10a, 19.11, 20.3b, 20.8b, 20.9, 21.4a, 21.7b, hearts in Mecoptera, pp. 63–76, 1993.
22.15b, 23.12c, 23.17c, 25.11b, 26.3c, 26.10b, 26.10c, Table Fig. 5.15. Reprinted from the Journal of Insect Physiology, 16,
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the American cockroach, pp. 331–40, 1970.
Cornell University Press Fig. 5.15. Reprinted from the Journal of Insect Physiology, 26,
Fig. 26.3a reprinted from Cricket Behavior and Neurobiology, S.W. Nicolson, Water balance and osmoregulation in
edited by Franz Huber, Thomas E. Moore, and Werner Loher; Onymacris, pp. 315–20, 1980.
original drawing by H.C. Bennett-Clark. Copyright 1989 by Fig. 5.20a,b. Reprinted from the Journal of Insect Physiology, 33,
Cornell University. Used by permission of the publisher, R.C. Duhamel & J.G. Kunkel, Moulting-cycle regulation of
Cornell University Press. haemolymph protein clearance in cockroaches, pp. 155–8,
1987.
Elsevier Science Ltd Fig. 5.20c. Reprinted from Insect Biochemistry and Molecular
With kind permission from Elsevier Science Ltd, The Boulevard, Biology, 15, L.M. Riddiford & R.H. Hice, Development
Langford Lane, Kidlington OX5 1GB, UK. profiles of the mRNAs for Manduca arylpghorin and two other
Fig. 3.3, 3.10b, 3.15, 3.16. Reprinted from G.A. Kerkut & L.I. storage proteins, pp. 489–502, 1985.
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Marchini, Ultrastructure of the midgut and adhering tubular Comprehensive Insect Physiology, Biochemistry and
salivary glands in Frankliniella, pp. 15–24, 1991. Pharmacology, 1985, vol. 3, pp. 155–310.
ACKNOWLEDGMENTS xv
Fig. 6.4. Reprinted from Insect Biochemistry and Molecular Fig. 14.30. Reprinted from Journal of Insect Physiology, 20, D.C.
Biology, 20, N.H. Haunerland, K.K. Nair & W.S. Bowers, Fat Denlinger & W.-C. Ma, Dynamics of the pregnancy cycle in
body heterogeneity during development of Heliothis zea, pp. the tsetse fly, pp. 1015–26, 1974.
829–37, 1990. Fig. 15.12a. Reprinted from the International Journal of Insect
Fig. 6.7. Reprinted from Comparative Biochemistry and Morphology & Embryology, 18, R.F. Chapman & J. Fraser, The
Physiology, 91A, A. Gies, T. Fromm & R. Ziegler, Energy chemosensory system of the monophagus grasshopper
metabolism in starving larvae of Manduca sexta, pp. 549–55, Bootettix, pp. 111–18, 1989.
1992. Fig. 15.35. Reprinted from the Journal of Insect Physiology, 36,
Fig. 8.28. Reprinted from the Journal of Insect Physiology, 41, D. A. Rachinsky & K. Hartfelder, Corpora allata activity, a prime
Berrigan & D.J. Pepin, How maggots move, pp. 329–337, 1995. regulating element for caste-specific juvenile hormone titre in
Fig. 8.31. Reprinted from G.A. Kerkut & L.I. Gilbert, honey bee larvae, pp. 189–94, 1990.
Comprehensive Insect Physiology, Biochemistry and Fig. 15.36. Reprinted from the Journal of Insect Physiology, 29,
Pharmacology, 1985, vol. 5, pp. 467–90. D.E. Wheeler & H.F. Nijhout, Soldier determination in
Fig. 10.1d. Reprinted from Progress in Biophysics and Molecular Pheidole, pp. 847–54, 1983.
Biology, 16, D.S. Smith, The organization and function of the Fig. 15.37. Reprinted from G.A. Kerkut & L.I. Gilbert, 1985,
sarcoplasmic reticulum and T-system of muscle cells, pp. Comprehensive Insect Physiology, Biochemistry and
109–42, 1966. Pharmacology, vol. 8, pp. 441–90.
Fig. 10.12. Reprinted from the Journal of Insect Physiology, 19, Fig. 15.43. Reprinted from the Journal of Insect Physiology,
M. Anderson & L.H. Finlayson, Ultrastructural changes 21, R.A. Bell, D.R. Nelson, T.K. Borg & D.L. Cardwell,
during growth of the flight muscles in the adult tsetse fly, pp. Wax secretion in non-diapausing and diapausing pupae of the
1989–97, 1973. tobacco hornworm, pp. 1725–9, 1975.
Fig. 10.15c. Reprinted from the Journal of Insect Physiology, 29, Fig. 16.19a. Reprinted from Insect Biochemistry and Molecular
W.K. Jorgensen & M.J. Rice, Superextension and Biology, 13, R.F. Ahmed, T.L. Hopkins & K.J. Kramer,
supercontraction in locust ovipositor muscles, pp. 437–48, 1983. Tyrosine and tyrosine glucoside titres in whole animals and
Fig. 12.4b. Reprinted from Journal of Insect Physiology, 35, A.K. tissues during development of the tobacco hornworm, pp.
Raina, Male-induced termination of sex pheromone 369–74, 1983.
production and receptivity in mated females of Heliothis zea, Fig. 17.17. Reprinted from the Journal of Insect Physiology, 34,
pp. 821–26, 1989. J.R.B. Lighton, Simultaneous measurement of oxygen uptake
Fig. 13.5a–c, 13.6. Reprinted from the International Journal of and carbon dioxide emission during discontinuous ventilation,
Insect Morphology & Embryology, 22, J. Büning, Germ cell pp. 361–7, 1988.
cluster formation in insect ovaries, pp. 237–53, 1993. Fig. 17.18. Reprinted from the Journal of Insect Physiology, 39,
Fig. 13.5d. Reprinted from International Journal of Insect J.R.B. Lighton, Ventilation in Cataglyphis bicolor, pp. 687–99,
Morphology & Embryology, 22, E. Huebner & W. Diehl-Jones, 1993.
Nurse cell-oocyte interaction in the telotrophic ovary, pp. Fig. 18.11b. Reprinted from the Journal of Insect Physiology,
369–87, 1993. 32, A.G. Appel, D.A. Reierson & M.K. Rust, Cuticular
Fig. 13.8a. Reprinted from the Journal of Insect Physiology, 33, water loss in the smokybrown cockroach, pp. 623–8,
M.J. Klowden, Distension-mediated egg maturation in the 1986.
mosquito Aedes aegypti, pp. 83–7, 1987. Fig. 18.15c. Reprinted from the Journal of Insect Physiology, 29,
Fig. 13.9c. Reprinted from Insect Biochemistry and Molecular D. Rudolph, The water-vapour uptake system of the
Biology, 8, G. Gellisen & H. Emmerich, Changes in the titer of Phthiraptera, pp. 15–25, 1983.
vitellogenin and of diglyceride carrier protein in the blood of Fig. 20.5c. Reprinted from G.A. Kerkut & L.I. Gilbert,
adult Locusta, pp. 403–12, 1978. Comprehensive Insect Physiology, Biochemistry and
Fig. 13.10d. Reprinted from the Journal of Insect Physiology, 36, Pharmacology, 1985, vol. 5, pp. 139–79.
C.-M. Yin, B.-X.Zou, S.-X.Yi & J.G. Stoffolano, Ecdysteroid Fig. 21.10b. Reprinted from Insect biochemistry and Molecular
activity during oogenesis in the black blowfly, Phormis regina Biology, 20, P. Jesudason, K. Venkatesh & R.M. Roe,
(Meigen), pp. 375–82, 1900. Haemolymph juvenile hormone esterase during the life cycle
Fig. 14.26c. Reprinted from the Journal of Insect Physiology, 25, of the tobacco hornworm, pp. 593–604, 1990.
M. Lagueux, C. Hetru, F. Goltzene, C. Kappler & J.A. Fig. 24.4. Reprinted from the Journal of Insect Physiology, 39, H.
Hoffmann, Ecdysone titre and metabolism in relation to Ljunberg, P. Anderson & B.S. Hansson, Physiology and
cuticulogenesis in embryos of Locusta migratoria, pp. 709–23, morphology of pheromone-specific sensilla on the antennae of
1979. male and female Spodoptera, pp. 253–90, 1993.
xvi ACKNOWLEDGMENTS
Fig. 24.10c. Reprinted from the Journal of Insect Physiology, 37, Plenum Press
L.M. Schoonhoven, M.S.J. Simmonds & W.M. Blaney, Figs. 10.2, 27.23b
Changes in the responsiveness of the maxillary styloconic
sensilla of Spodoptera, pp. 261–68, 1991. Royal Entomological Society
Fig. 25.12. Reprinted from Insect Biochemistry and Molecular Figs. 3.2, 25.18
Biology, 21, P.B. Koch, Precursors of pattern specific ommatin
Royal Society of London
in red wing scales of the polyphenic butterfly Araschia levana,
Fig. 9.18b–d from J.A. Miyan & A.W. Ewing, Philosophical
pp. 7853–94, 1991.
Transactions of the Royal Society of London, B 311, 1985,
Elsevier Trends Journals 271–302, Fig. 5.
Fig. 8.20 from M. Burrows, Local circuits for the control of leg Fig. 9.29b from C.P. Ellington, Philosophical Transactions of the
movements in an insect, Trends in Neuroscience, 15, 226–32, 1992. Royal Society of London, B 305, 1984, 79–113, Fig. 6b.
Fig. 17.5 from M. Burrows, Proceedings of the Royal Society of
Entomological Society of America London, B 207, 1980, 63–78, Fig. 2.
Figs. 3.2c, 15.11, 17.33b, 26.2 Fig. 20.18 from L. Pearson, Philosophical Transactions of
the Royal Society of London, B 259, 1974, 477–516, Fig. 32.
Entomological Society of British Colombia Fig. 20.23 from S.G. Matsumoto & J.G. Hildebrand, Proceedings
Fig. 16.9 of the Royal Society of London, B 213, 1981, 249–77, Fig. 26.
Fig. 24.12b from V.O.C. Shields & B.K. Mitchell, Philosophical
Entomological Society of Canada Transactions of the Royal Society of London, B 347, 1995,
Fig. 5.6h 459–64, Fig. 1c.
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Evolution Society of London, B 226, 1985, 367–90, Fig. 6.
Fig. 19.6
E. Schweizerbart’sche Verlagsbuchhandlung
Fig. 3.10c
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Fig. 15.12b. Figure 1A, Pflüger et al., Activity-dependent
Society for Integrative and Comparative Biology
structural dynamics of insect sensory fibers. The Journal of
Figs. 3.26b, 21.12
Neuroscience, 14(11): 6948, (1994).
Fig. 15.23b. Figures 1A, 1D, Truman & Reiss, Hormonal
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regulation of the shape of identified motor neurons in the moth
Fig. 9.21 From A.K. Brodsky, The Evolution of Insect Flight,
Manduca sexta. The Journal of Neoroscience, 8(3): 766, (1988).
1994, by permission.
Verlag der Zeitschrift fur Naturforschung Fig. 18.13 from Simultaneous measurements of evaporative
Fig. 15.26 water loss, oxygen consumption, and thoracic temperature
during flight, S.W. Nicholson & G.N. Louw, Journal of
John Wiley & Sons, Inc Experimental Zoology, 1982.
Reprinted by Permission of Wiley–Liss, Inc., a subsidiary of John Fig. 18.15a,b from Novel uptake systems for atmospheric water
Wiley & Sons, Inc. vapor, D. Rudolph & W. Knulle, Journal of Experimental
Fig. 5.6e–g from Gross and fine structure of the antennal Zoology, 1982.
circulatory organ in cockroaches, G. Pass, Journal of Fig. 20.2a from Synaptic organization of columnar elements in
Morphology, 1985. the lamina of the wild type in Drosophila, I.A.
Fig. 5.24 from Water compartmentalization in insects, J. Machin, Meinertzhagen & S.D. O’Neil, Journal of Comparative
Journal of Experimental Zoology, 1981. Neurology, 1991.
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Gupta & S.S. Han, Journal of Morphology, 1988. nonspiking local interneurons in the thoracic nervous system
Fig. 10.10a from Flight muscle development in a of the locust, A.H.D. Watson & M. Burrows, Journal of
hemimetabolous insect, N.E. Ready & R.K. Josephson, Journal Comparative Neurology, 1988.
of Experimental Zoology, 1962. Fig. 20.12 from The morphology of nonspiking interneurons in
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Zoology, 1986. Fig. 20.15 from Heterogeneous properties of segmentally
Fig. 10.17a from Extensive and intensive factors determining the homologous interneurones in the ventral nerve cords of
performance of striated muscle, R.K. Josephson, Journal of locusts, K.G. Pearson, G.S. Boyan, M. Bastiani & C.S.
Experimental Zoology, 1985. Goodman, Journal of Comparative Neurology, 1985.
Fig. 12.2a from Cytodifferentiation in the accessory glands of Fig. 20.20 from Neuroarchitecture of the central complex in the
Tenebrio molitor VI, P.J. Dailey, N.M. Gadzama & G.M. Happ, brain of the locust, U. Homberg, Journal of Comparative
Journal of Morphology, 1980. Neurology, 1991.
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Drosophila, P.J. Bryant, Journal of Experimental Zoology, 1975. locust interneurones, their dendritic morphology and
Fig. 15.23c from Postembryonic neurogenesis in the CNS of the the central projections of mechanosensory neurones, M.
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during metamorphosis, V.W. Russell & P.E. Dunn, Archives of in the prothoracic glands of Manduca sexta, W.S. Smith,
Insect Biochemistry and Physiology, 1991. Archives of Insect Biochemistry and Physiology, 1995.
PART I
Insects and other arthropods are built up on a segmental gnathal segments because their appendages form the
plan and their characteristic feature is a hard, jointed mouthparts of the insect.
exoskeleton. The cuticle, which forms the exoskeleton, is Reviews: Bitsch, 1973; Denis & Bitsch, 1973; DuPorte, 1957;
continuous over the whole of the outside of the body and Matsuda, 1965; Snodgrass, 1935, 1960
consists of a series of hard plates, the sclerites, joined to
each other by flexible membranes, which are also cuticular. 1.1.1 Orientation
Sometimes the sclerites are articulated together so as to The orientation of the head with respect to the rest of the
give precise movement of one on the next. Each segment body varies (Fig. 1.1). The hypognathous condition, with
of the body primitively has a dorsal sclerite, the tergum, the mouthparts in a continuous series with the legs, is
joined to a ventral sclerite, the sternum, by lateral mem- probably primitive. This orientation occurs most com-
branous areas, the pleura. Arising from the sternopleural monly in phytophagous species living in open habitats. In
region on each side is a jointed appendage. the prognathous condition the mouthparts point forwards
In insects, the segments are grouped into three units, and this is found in predaceous species that actively pursue
the head, thorax and abdomen, in which the various basic their prey, and in larvae, particularly of Coleoptera, which
parts of the segments may be lost or greatly modified. use their mandibles in burrowing. In Hemiptera, the elon-
Typical walking legs are only retained on the three thoracic gate proboscis slopes backwards between the forelegs.
segments. In the head, the appendages are modified for This is the opisthorhynchous condition.
sensory and feeding purposes and in the abdomen they are The mouthparts enclose a cavity, the pre-oral cavity,
lost, except that some may be modified as the genitalia and with the mouth at its inner end (Fig. 1.2). The part of the
in Apterygota some pregenital appendages are retained. pre-oral cavity enclosed by the proximal part of the hypo-
pharynx and the clypeus is known as the cibarium. Between
the hypopharynx and the labium is a smaller cavity known
1.1 HEAD
as the salivarium, into which the salivary duct opens.
The insect head is a strongly sclerotized capsule joined to
the thorax by a flexible membranous neck. It bears the 1.1.2 Rigidity
mouthparts, comprising the labrum, mandibles, maxillae The head is a continuously sclerotized capsule with no
and labium, and also important sense organs, the antennae, outward appearance of segmentation, but it is marked by a
compound eyes and ocelli. On the outside it is marked by number of grooves. Most of these grooves are sulci (singu-
grooves most of which indicate ridges on the inside, and lar: sulcus), marking lines along which the cuticle is
some of these inflexions extend deep into the head, fusing inflected to give increased rigidity. The term suture should
with each other to form an internal skeleton. These struc- be retained for grooves marking the line of fusion of two
tures serve to strengthen the head and provide attach- formerly distinct plates. The groove which ends between
ments for muscles as well as supporting and protecting the the points of attachment of maxillae and labium at the back
brain and foregut. of the head is generally believed to represent the line of
The head is derived from the primitive pre-oral fusion of the maxillary and labial segments and it is there-
archecerebrum and a number of primitively post-oral seg- fore known as the postoccipital suture.
ments. Molecular studies of Drosophila suggest that there Since the sulci are functional mechanical developments
are seven postoral segments: labral, ocular, antennal, inter- to resist the various strains imposed on the head capsule,
calary, mandibular, maxillary and labial (Schmidt-Ott et they are variable in position in different species and any
al., 1994). The last three segments are often called the one of them may be completely absent. However, the needs
[3]
4 HEAD
a) hypognathous
brain
frons
pharynx
antenna
salivary duct
mandible
pharyngeal
maxillary dilator subesophageal
palp mesothoracic muscles ganglion
leg frontal ganglion
labial suspensory
palp sclerite
prothoracic
leg mouth
salivarium
cibarium
lingual
b) prognathous sclerite
clypeus
antenna labium
labrum
mandible
epipharynx hypopharynx
labial
Fig. 1.2. Pre-oral cavity and some musculature. Diagrammatic
maxillary
palp palp vertical section through the head of an insect with biting and
chewing mouthparts. Sclerites associated with the hypopharynx
prothoracic are black with white spots. Muscles attached to these sclerites
leg move the hypopharynx (after Snodgrass, 1947).
a) anterior b) lateral
occipital sulcus
ecdysial line
postoccipital
suture
postocciput
neck
circumocular sulcus membrane
post- subgenal
circumantennal sulcus sulcus
gena gena
frons subocular sulcus frons gena posterior
anterior tentorial pit tentorial pit
clypeus subgena
anterior epistomal sulcus
articulation of mandible labium
mandible labrum
maxilla
Fig. 1.3. Common lines or grooves on the insect head and the areas which they define (italicized) (modified after Snodgrass,
1960).
too are the areas which they delimit. The front of the head, membrane, articulating with the subgena on either side.
the frontoclypeal area, is divided by the epistomal sulcus into The hypostomal sulci bend upwards posteriorly and are
the frons above and the clypeus below (Fig. 1.3). It is continuous with the postoccipital suture (Fig. 1.4a). In
common to regard the arms of the ecdysial cleavage line as insects with a narrow neck, permitting greater mobility of
delimiting the frons dorsally, but this is not necessarily so the head, and in prognathous insects, the cuticle of the
(Snodgrass, 1960). From the frons, muscles run to the head below the occipital foramen is sclerotized. This
pharynx, the labrum and the hypopharynx; from the clypeus region has different origins. In Diptera, the hypostomata
arise the dilators of the cibarium. The two groups of muscles of the two sides meet in the midline below the occipital
are always separated by the frontal ganglion and its connec- foramen to form a hypostomal bridge which is continuous
tives to the brain (Fig. 1.2). Dorsally the frons continues into with the postocciput (Fig. 1.4b). In other cases,
the vertex and posteriorly this is separated from the occiput Hymenoptera and the water bugs Notonecta and Naucoris,
by the occipital sulcus. The occiput is divided from the post- a similar bridge is formed by the postgenae, but the bridge
occiput behind it by the postoccipital suture, while at the is separated from the postocciput by the postoccipital
back of the head, where it joins the neck, is an opening, the suture (Fig. 1.4c). Where the head is held in the prog-
occipital foramen, through which the alimentary canal, nathous position, the lower ends of the postocciput fuse
nerve cord and some muscles pass into the thorax. and extend forwards to form a median ventral plate, the
The lateral area of the head beneath the eyes is called gula (Fig. 1.4d), which may be a continuous sclerotization
the gena, from which the subgena is cut off below by the with the labium. Often the gula is reduced to a narrow strip
subgenal sulcus, and the postgena behind by the occipital by enlargement of the postgenae and sometimes the post-
sulcus. The region of the subgena above the mandible is genae meet in the midline, so that the gula is obliterated.
called the pleurostoma and that part behind the mandible The median ventral suture which is thus formed at the
is the hypostoma. point of contact of the postgenae is called the gular suture.
In hypognathous insects with a thick neck, the poste- In all insects, the rigidity of the head is increased by
rior ventral part of the head capsule is membranous. The four deep cuticular invaginations, known as apodemes,
postmentum of the labium is contiguous with this which usually meet internally to form a brace for the head
6 HEAD
c) postgenal bridge
postoccipital
suture occipital
foramen
postocciput
posterior
tentorial pit
gula
postgena
postgenal hypostomal
bridge sulcus submentum
subgena
labium mentum
maxilla
mandible
and for the attachment of muscles. The structure formed 1.1.3 Molting
by these invaginations is called the tentorium (Fig. 1.5). Immature insects nearly always have a line along the dorsal
Its two anterior arms arise from the anterior tentorial pits, midline of the head dividing into two lines on the face so as to
which in Apterygota and Ephemeroptera are ventral and form an inverted Y (Fig. 1.3). There is no groove or ridge
medial to the mandibles. In Odonata, Plecoptera and along this line, and it is simply a line of weakness, continuous
Dermaptera the pits are lateral to the mandibles, while in with that on the thorax, along which the cuticle splits when
most higher insects they are facial at either end of the epis- the insect molts (see Fig. 16.11). It is therefore called the
tomal sulcus. The posterior arms arise from pits at the ecdysial cleavage line, but has commonly been termed the
ventral ends of the postoccipital suture and they unite to epicranial suture. The anterior arms of this line are very vari-
form a bridge running across the head from one side to the able in their development and position and, in Apterygota,
other. In Pterygota the anterior arms also join up with the they are reduced or absent. The ecdysial cleavage line may
bridge, but the development of the tentorium as a whole is persist in the adult insect and sometimes the cranium is
very variable. Sometimes a pair of dorsal arms arise from inflected along this line to form a true sulcus. Other ecdysial
the anterior arms and they may be attached to the dorsal lines may be present on the ventral surface of the head of
wall of the head by short muscles. In Machilidae larval insects (Hinton, 1963).
(Archaeognatha) the posterior bridge is present, but the
anterior arms do not reach it, while in Lepismatidae 1.2 NECK
(Thysanura) the anterior arms unite to form a central The neck or cervix is a membranous region which gives
plate near the bridge and are joined to it by very short freedom of movement to the head. It extends from the post-
muscles. occiput at the back of the head to the prothorax, and possibly
NECK 7
postocciput
occipital
condyle
b) head movement
head retracted head protracted
cervical
cervical sclerites
sclerites
8 HEAD
a) annulated b) segmented
pedicel
flagellum scape flagellum
extensor
muscle pedicel
annuli
flexor levator
muscles muscle
scape
depressor intrinsic muscles
muscle of flagellar
segments
extensor
flexor muscles
muscles
levator
muscle
Fig. 1.7. Antenna. Proximal region showing the musculature. (a) Typical insect annulated antenna. There are no muscles in
the flagellum (Locusta, Orthoptera). (b) Segmented antenna of a non-insect hexapod (Japyx, Diplura) (after Imms, 1940).
represents the posterior part of the labial segment together fiber. This polyneuronal innervation, together with the
with the anterior part of the prothoracic segment. Laterally versatility of the cervical articulations and the complexity
in the neck membrane are the cervical sclerites. Sometimes of the musculature, permits movement of the head in a
there is only one, as in Ephemeroptera, but there may be two highly versatile and accurately controlled manner.
or three. In Schistocerca (Orthoptera) the first lateral cervical
sclerite, which articulates with the occipital condyle at the
1.3 ANTENNAE
back of the head, is very small. The second sclerite articulates
with it by a ball and socket joint allowing movement in all All insects possess a pair of antennae, but they may be
planes. Posteriorly it meets the third (posterior) cervical scle- greatly reduced, especially in larval forms. Amongst the
rite and movement at this joint is restricted to the vertical non-insectan Hexapoda, Collembola and Diplura have
plane. The third cervical sclerite connects with the protho- antennae, but Protura do not.
racic episternum, relative to which it can move in all planes.
Muscles arising from the postocciput and the pro- 1.3.1 Antennal structure
notum are inserted on the cervical sclerites (Fig. 1.6a) and The antenna consists of a basal scape, a pedicel and a
their contraction increases the angle between the sclerites flagellum. The scape is inserted into a membranous region
so that the head is pushed forwards (Fig. 1.6b). A muscle of the head wall and pivoted on a single marginal point, the
arising ventrally and inserted on to the second cervical antennifer (Fig. 1.8a), so it is free to move in all directions.
sclerite may aid in retraction or lateral movements of the Frequently the flagellum is divided into a number of similar
head. Running through the neck are longitudinal muscles, annuli joined to each other by membranes so that the
dorsal muscles from the antecostal ridge of the mesothorax flagellum as a whole is flexible. The term segmented should
to the postoccipital ridge, and ventral muscles from the be avoided with reference to the flagellum of insects since
sternal apophyses of the prothorax to the postoccipital the annuli are not regarded as equivalent to leg segments.
ridge or the tentorium. These muscles serve to retract the The antennae of insects are moved by levator and
head on to the prothorax, while their differential contrac- depressor muscles arising on the anterior tentorial arms and
tion will cause lateral movements of the head. Schistocerca inserted into the scape, and by flexor and extensor muscles
has 16 muscles on each side of the neck, each of which is arising in the scape and inserted into the pedicel (Fig. 1.7a).
innervated by several axons, often including an inhibitory There are no muscles in the flagellum, and the nerve which
ANTENNAE 9
flagellum
antennifer part of
head
capsule
pedicel
pedicel
scape
scape
e) Lepidopteran
d) cyclorraphous scape larva
Diptera
pedicel
arista
basal
annulus pedicel
scape
traverses the flagellum is purely sensory. This is the annu- number increases at each molt (see Fig. 15.10). In
lated type of antenna. In Collembola and Diplura the mus- Periplaneta, for example, there are only 48 annuli in the
culature at the base of the antenna is similar to that in first stage larva compared with over 150 in the adult. The
insects, but, in addition, there is an intrinsic musculature in antennae of larval holometabolous insects are usually
each unit of the flagellum (Fig. 1.7b), and, consequently, considerably different from those of the adult. The larval
these units are regarded as true segments. antennae of Neuroptera and Megaloptera have a number
The number of annuli is very variable between species. of annuli, but in larval Coleoptera and Lepidoptera the
Adult Odonata, for example, have five or fewer annuli antennae are reduced to three simple segments. In some
while adult Periplaneta have over 150, increasing from larval Diptera and Hymenoptera the antennae are very
about 48 in the first stage larva. small and may be no more than swellings of the head wall.
The form of the antenna varies considerably depend-
ing on its precise function (Fig. 1.8). Sometimes the 1.3.2 Sensilla on the antennae
modification produces an increase in surface area allowing The antennae are primarily sensory structures and they are
a large number of sensilla to be accommodated on the richly endowed with sensilla in most insects. It is character-
antenna (Fig. 1.9) and, in the case of the plumose antennae istic of insects that the pedicel contains a chordotonal organ,
of some male moths, enabling them to sample a large Johnston’s organ, which responds to movement of the
volume of air. Sexual dimorphism in the antennae is flagellum with respect to the pedicel (see section 23.2.3.2).
common, those of the male often being more complex than In addition, the scape and pedicel often have hair plates and
those of the female. This often occurs where the male is groups of campaniform sensilla that provide information on
attracted to or recognizes the female by her scent. the positions of the basal segments with respect to the head
Conversely, in chalcids scent plays an important part in and to each other. Scattered mechanosensory hairs are also
host-finding by the female and in this case the female’s often present on these segments.
antennae are more specialized than the male’s. The principal sensilla on the flagellum of most insects are
The antennae of larval hemimetabolous insects are olfactory, and these have a variety of forms (see section 24.1.1).
similar to those of the adult, but with fewer annuli. The It is common for contact chemoreceptors, mechanoreceptors
10 HEAD
flagellum
pedicel trichoid
sensilla
scape
annulus basal part
20 of branch
and thermohygroreceptors also to be present. Where the mosquitoes, female Drosophila and worker honeybees, for
flagellum is made up of a series of similar annuli, successive example, it is concerned in the perception of near-field
annuli often have a similar arrangement of sensilla, but the sen- sounds (see Fig. 23.11).
silla are often concentrated in particular regions. In Melanoplus Sometimes the antennae have other functions. The adult
(Orthoptera), for instance, there are no basiconic or coeloconic water beetle Hydrophilus submerges with a film of air over
pegs on the proximal annuli; most of these sensilla are found on its ventral surface which it renews at intervals when it comes
the annuli in the middle of the flagellum (Fig. 1.10). In Pieridae to the surface. At the water surface the body is inclined to
(Lepidoptera), most of the antennal sensilla are aggregated on one side and a funnel of air, connecting the ventral air
the terminal club. The terminal annulus often has a group of bubble to the outside air, appears between the head, the pro-
contact chemoreceptors at its tip. The total numbers of sensilla thorax and the distal annuli of the antenna, which is held
on an antenna are often very large. Adult male Periplaneta, for along the side of the head. The four terminal annuli of the
instance, have about 250 000 sensilla on each antenna and male antenna are enlarged and are clothed with hydrofuge hairs
corn borer moths, Ostrinia, about 8000. When the antennae are
sexually dimorphic, as in many Lepidoptera, the more complex
antenna bears a much larger number of sensilla. For example, 200
male Telea have over 65 000 sensilla on one antenna, while the basiconic
number of sensilla
sensilla
female has only about 13 000. 150
Review: Zacharuk, 1985
100
1.3.3 Functions of antennae coeloconic
50
The antennae function primarily as sense organs and they sensilla
are the primary olfactory receptors of all insects (see 0
section 24.1.1). They also have a tactile function by virtue 5 10 15 20 25
of the large number of mechanosensitive sensilla that are annulus number
often present. Very long antennae, such as occur in the Fig. 1.10. Distribution of sensilla along the flagellum of a male
cockroach, are possibly associated with their use as feelers. grasshopper. Only olfactory sensilla are shown. 1 ⫽most
Johnston’s organ is important in the regulation of airspeed proximal annulus, adjacent to the pedicel; 25 ⫽most distal
in flying insects (see Fig. 9.36) and in some insects, male annulus (Melanoplus) (data from Slifer et al., 1959).
REFERENCES 11
which facilitate the formation of the air funnel. In the newly on stalks above the general surface of the cuticle and
hatched larva of Hydrophilus the antennae assist the within each one there is a gland, presumably secreting an
mandibles in masticating the prey. This is facilitated by a adhesive material. Species with sessile or semi-sessile
number of sharp spines on the inside of the antennae. females lack these organs (Rothschild and Hinton, 1968).
In fleas and Collembola the antennae are used in In many Collembola the males have prehensile antennae
mating. Male fleas use the antennae to clasp the female with which they hold on to the antennae of the female and,
from below and the inner surfaces bear large numbers of in Sminthurides aquaticus, the male may be carried about by
adhesive discs. These discs, about 5 m in diameter, are set the female, holding on to her antennae, for several days.
REFERENCES
Bitsch, J. (1973). Morphologie de la tête des Imms, A.D. (1940). On the antennal Slifer, E.H., Prestage, J.J. & Beams, H.W.
insectes. A. Partie Générale. In Traité de structure in insects and other arthro- (1959). The chemoreceptors and other
Zoologie, vol. 8, part 1, ed. P.-P.Grassé, pods. Quarterly Journal of Microscopical sense organs on the antennal flagellum
pp. 3–100. Paris: Masson et Cie. Science, 81, 273–320. of the grasshopper, (Orthoptera:
Boeckh, J., Kaissling, K.-E. & Schneider, Imms, A.D. (1957). A General Textbook of Acrididae). Journal of Morphology, 105,
D. (1960). Sensillen und Bau der Entomology. London: Methuen. 145–91.
Antennengeissel von Telea polyphemus. Matsuda, R. (1965). Morphology and Snodgrass, R.E. (1935). Principles of Insect
Zoologische Jahrbücher (Anatomie), 78, evolution of the insect head. Memoirs of Morphology. New York: McGraw-Hill.
559–84. the American Entomological Institute, no. Snodgrass, R.E. (1947). The insect
Denis, J.R. & Bitsch, J. (1973). 4, 334 pp. cranium and the ‘epicranial suture’.
Morphologie de la tête des insectes. B. Rothschild, M. & Hinton, H.E. (1968). Smithsonian Miscellaneous Collections,
Structure céphalique dans les ordres Holding organs on the antennae of 104, no. 7, 113 pp.
d’insectes. In Traité de Zoologie, vol. 8, male fleas. Proceedings of the Royal Snodgrass, R.E. (1960). Facts and theories
part 1, ed. P.-P.Grassé, pp. 101–593. Entomological Society of London, (A) 43, concerning the insect head.
Paris: Masson et Cie. 105–7. Smithsonian Miscellaneous Collections,
DuPorte, E.M. (1957). The comparative Schmidt-Ott, U., González-Gaitán, M., 142, 1–61.
morphology of the insect head. Annual Jäckle, H. & Technau, G.M. (1994). Zacharuk, R.Y. (1985). Antennae and sen-
Review of Entomology, 2, 55–70. Number, identity, and sequence of the silla. In Comprehensive Insect
Hinton, H.E. (1963). The ventral ecdysial Drosophila head segments as revealed Physiology, Biochemistry and
lines on the head of endopterygote by neural elements and their deletion Pharmacology, vol. 6, ed. G.A. Kerkut
larvae. Transactions of the Royal patterns in mutants. Proceedings of the & L.I. Gilbert, pp. 1–69. Oxford:
Entomological Society of London, 115, National Academy of Sciences of the Pergamon Press.
39–61. United States of America, 91, 8363–7.
2 Mouthparts and feeding
The mouthparts are the organs concerned with feeding, may be produced into a median lobe, the epipharynx,
comprising the unpaired labrum in front, a median hypo- bearing some sensilla. The labrum is raised away from the
pharynx behind the mouth, a pair of mandibles and maxil- mandibles by two muscles arising in the head and inserted
lae laterally, and a labium forming the lower lip. In medially into the anterior margin of the labrum. It is closed
Collembola, Diplura and Protura the mouthparts lie in a against the mandibles in part by two muscles arising in the
cavity of the head produced by the genae, which extend head and inserted on the posterior lateral margins on two
ventrally as oral folds and meet in the ventral midline small sclerites, the tormae, and, at least in some insects, by a
below the mouthparts (Fig. 2.1). This is the entognathous resilin spring in the cuticle at the junction of the labrum
condition. In the Insecta the mouthparts are not enclosed with the clypeus. Differential use of the muscles can
in this way, but are external to the head, the ectognathous produce a lateral rocking movement of the labrum.
condition.
Mandibles In the entognathous groups and the
Archaeognatha, the mandibles are relatively long and
2.1 ECTOGNATHOUS MOUTHPARTS
slender and they have only a single point of articulation
The form of the mouthparts is related to diet, but two with the head capsule (Fig. 2.3). The mandible is rotated
basic types can be recognized: one adapted for biting and about its articulation by anterior and posterior muscles
chewing solid food, and the other adapted for sucking up arising on the head capsule and on the anterior tentorial
fluids. arms. The principal adductor muscles are transverse and
ventral, those of the two sides uniting in a median tendon.
2.1.1 Biting mouthparts In Thysanura and the Pterygota, the mandibles are
articulated with the cranium at two points, having a second
Labrum The labrum is a broad lobe suspended from the more anterior articulation with the subgena in addition to
clypeus in front of the mouth and forming the upper lip the original posterior one (Figs. 1.3, 2.2b). These
(Figs. 1.2, 2.2a). On its inner side it is membranous and mandibles are usually short and strongly sclerotized and
esophagus mandible
labrum
mandible
superlingua
cavity enclosed
by oral folds maxilla
maxilla hypopharynx
oral fold hypopharynx oral fold cavity enclosed
A by oral folds
Fig. 2.1. Entognathous mouthparts (modified after Denis, 1949). (a) Lateral view showing the mouthparts within the cavity
formed by the oral folds. The extent of the cavity is indicated by hatching. (b) Transverse section at AA in (a).
[12]
a) labrum b) mandible
anterior
muscles adductor abductor
muscle muscle
posterior
muscle
points of
articulation
torma inside of
mandible
lacinea
lacinea flexor muscle
galea of galea
galea
palp
d) labium
points of
articulation with
head capsule
muscles to
prementum
from tentorium
retractor muscle
of prementum
submentum postmentum
levator muscle
of palp
mentum intrinsic muscles depressor muscle
of palp of palp
prementum
flexor muscle
of paraglossa
palp flexor muscle
of glossa
paraglossa
glossa
Fig. 2.2. Biting and chewing mouthparts of a pterygote insect. Surfaces normally in contact with the hemocoel, the inside of
the cuticle, are shaded (after Snodgrass, 1935, 1944). (a) Labrum seen from the posterior, epipharyngeal, surface . (b)
Mandible, notice the dicondylic articulation. (c) Maxilla from the outside (left) and inside (right). (d) Labium from the
outside (left) and inside (right).
14 MOUTHPARTS AND FEEDING
anterior rotator lacinea nor galea has an extensor muscle. The palp has
muscle
levator and depressor muscles arising in the stipes and
posterior rotator
muscle each segment of the palp has a single muscle causing
flexing of the next segment.
condyle
remotor
muscle Labium The labium is similar in structure to the maxillae,
ventral adductor but with the appendages of the two sides fused in the
muscle midline so that they form a median plate (Fig. 2.2d). The
median tendon basal part of the labium, equivalent to the maxillary car-
anterior tentorial dines and possibly including a part of the sternum of the
arm labial segment, is called the postmentum. This may be
mandible subdivided into a proximal submentum and a distal
mentum. Distal to the postmentum, and equivalent to the
Fig. 2.3. Monocondylic mandibles as found in Archaeognatha fused maxillary stipites, is the prementum. The pre-
and non-insectan hexapods. Not all muscles are shown (after mentum closes the pre-oral cavity from behind.
Snodgrass, 1935).
Terminally it bears four lobes, two inner glossae and two
outer paraglossae, which are collectively known as the
the cuticle of the cusps is often hardened by the presence ligula. One or both pairs of lobes may be absent or they
of zinc or manganese (see Fig. 16.9). These cusps may may be fused to form a single median process. A palp arises
become worn down during feeding, but the distribution of from each side of the prementum, often being three-
the harder areas of cuticle promotes self-sharpening segmented.
(Chapman, 1995). The musculature corresponds with that of the maxil-
The original anterior and posterior rotator muscles of lae, but there are no muscles to the postmentum. Muscles
Apterygota have become abductors and adductors in the corresponding with the ventral adductors run from the
Pterygota, the adductor often becoming very powerful. tentorium to the front and back of the prementum; glossae
The apterygote ventral adductor is retained in most and paraglossae have flexor muscles, but no extensors, and
orthopteroids and arises from the hypopharyngeal the palp has levator and depressor muscles arising in the
apophysis, but in Acrididae and the higher insects this prementum. The segments of the palp each have flexor
muscle is absent, or, in insects with sucking mouthparts, and extensor muscles. In addition, there are other muscles
may be modified as a protractor muscle of the mandible. with no equivalent in the maxillae. Two pairs arising in the
prementum converge on to the wall of the salivarium at the
Maxillae The maxillae occupy a lateral position, one on junction of labium with hypopharynx (Fig. 1.2). A pair of
each side of the head behind the mandibles. The proximal muscles opposing these arises in the hypopharynx and the
part of the maxilla consists of a basal cardo, which has a combined effect of them all may be to regulate the flow of
single articulation with the head, and a flat plate, the stipes, saliva or to move the prementum. Finally, a pair of muscles
hinged to the cardo (Fig. 2.2c). Both cardo and stipes are arising in the postmentum and inserted into the pre-
loosely joined to the head by membrane so that they are mentum serves to retract or flex the prementum.
capable of movement. Distally on the stipes are two lobes,
an inner lacinea and an outer galea, one or both of which Hypopharynx The hypopharynx is a median lobe
may be absent. More laterally on the stipes is a jointed, leg- immediately behind the mouth (Fig. 1.2). The salivary
like palp made up of a number of segments; in Orthoptera duct usually opens behind it, between it and the labium.
there are five. Most of the hypopharynx is membranous, but the adoral
Anterior and posterior rotator muscles are inserted on face is sclerotized distally, and proximally contains a pair of
the cardo, and ventral adductor muscles arising on the suspensory sclerites which extend upwards to end in the
tentorium are inserted on both cardo and stipes. Arising in lateral wall of the stomodeum. Muscles arising on the
the stipes are flexor muscles of lacinea and galea and frons are inserted into these sclerites, which distally are
another lacineal flexor arises in the cranium, but neither hinged to a pair of lingual sclerites. These, in turn, have
ECTOGNATHOUS MOUTHPARTS 15
inserted into them antagonistic pairs of muscles arising on liquid can be drawn into the mouth and usually another
the tentorium and labium. The various muscles serve to through which saliva passes. The muscles of the cibarium
swing the hypopharynx forwards and back, and in the or pharynx are strongly developed to form a pump. In
cockroach there are two more muscles running across the Hemiptera and many Diptera, which feed on fluids within
hypopharynx which dilate the salivary orifice and expand plants or animals, some components of the mouthparts are
the salivarium. modified for piercing, and the elongate structures are
In Apterygota, larval Ephemeroptera and Dermaptera called stylets. The combined tubular structures are
there are two lateral lobes of the hypopharynx called the referred to as the proboscis, although specialized terminol-
superlinguae. ogy is used in some groups.
In Hemiptera, mandibles, maxillae and labium are all
2.1.2 Variation in form elongate structures, while the labrum is relatively short.
The form of the mouthparts varies greatly between The food canal is formed by the opposed maxillae which
species. The biting surface of the mandible is often are held together by a system of tongues and grooves (Figs.
differentiated into a more distal incisor region and a proxi- 2.4a, 2.8a). These allow the stylets to slide freely on each
mal molar region whose development varies with diet. The other, while maintaining the integrity of the food canal.
mandibles of carnivorous insects are armed with strong The maxillae also contain the salivary canal. On either side
shearing cusps; in grasshoppers feeding on vegetation of the maxillae are the mandibular stylets. These are the
other than grasses, there is a series of sharp pointed cusps, principal piercing structures and they are often barbed at
while in grass-feeding species the incisor cusps are chisel- the tip. When the insect is not feeding, the slender maxil-
edged and the molar area has flattened ridges for grinding. lary and mandibular stylets are held within a groove down
In species that do not feed as adults, the mouthparts may the anterior side of the labium. The hemipteran labium is
be greatly reduced. The mandibles of adult known as the rostrum. It is usually segmented, allowing it
Ephemeroptera, for example, are vestigial or absent alto- to fold as the stylets penetrate the host. There are no palps.
gether and the maxillae and labium are also greatly Since the Hemiptera are hemimetabolous, the larvae and
reduced, being represented mainly by the palps. adults have similar feeding habits and both have sucking
The greatest divergence from the basic form occurs in mouthparts.
the larvae of holometabolous insects. While larval Thysanoptera are also fluid feeders as larvae and adults.
Lepidoptera and Coleoptera usually have well-developed Their stylets are normally held in the cone-shaped lower
biting and chewing mouthparts, larval Diptera and part of the head formed by the clypeus, the labrum and
Hymenoptera show some extreme modifications and labium. Only the left mandible is present. It is used to pen-
reductions. Mosquito larvae, for example, have brushes of etrate plant cells. The maxillary stylets are held together to
hairs on the mandibles and maxillae which are especially form the food canal. There is no salivary canal; the salivary
long in some species where they serve to filter particulate duct opens into the front of the esophagus (Chisholm &
material, including food, from the water. The larvae of Lewis, 1984).
cyclorrhaphous flies exhibit extreme reduction of the The adult Diptera exhibit a great variety of
head. The principal structures are a pair of heavily sclero- modifications of the mouthparts, but in all of them the
tized mouthhooks with which the larva rasps at its food; food canal is formed between the apposed labrum and
sensory papillae probably represent the palps. Amongst labium and the salivary canal runs through the hypo-
Hymenoptera, larval Symphyta have well-developed pharynx (Fig. 2.4e,f). The mandibles and maxillae are
mouthparts, similar to caterpillars, but in some parasitic styliform in species that suck the blood of vertebrates, but
species the mandibles are represented only by simple are generally lacking in other species, including the blood-
spines, and other mouthparts are not differentiated into sucking Cyclorrhapha. Where they are present, they are
separate sclerites. the piercing organs; in blood-sucking Cyclorrhapha tooth-
like structures at the tip of the labium penetrate the host
2.1.3 Sucking mouthparts tissues by a rasping action. Similar prestomal teeth occur
The mouthparts of insects which feed on fluids are in other Cyclorrhapha, including the house fly, Musca. In
modified in various ways to form a tube through which many species, the tip of the labium is expanded to form a
16 MOUTHPARTS AND FEEDING
a) Hemiptera b) Siphonaptera
food canal
mandible epipharynx
food canal
maxilla
maxilla
salivary canal
labium
salivary canal
d) Hymenoptera - Apidae
c) Lepidoptera food canal
food canal
maxilla
(galea)
maxilla labium
(galea) (glossa)
salivary canal
labium
(palp)
e) Diptera - Ceratopogonidae
f) Diptera - Glossinidae
labrum labrum
food canal
food canal
mandible
maxilla hypopharynx
Fig. 2.4. Sucking mouthparts. Diagrammatic cross-sections of the proboscis showing the principal structures used to form
tubes for delivery of saliva and intake of food. Homologous structures are indicated with the same shading in all the diagrams.
In some cases the structures contain an extension of the hemocoel; this is not shown. (a) Hemiptera (bugs) (compare Fig.
2.8a); (b) Siphonaptera (fleas); (c) Lepidoptera (butterflies and moths); (d) Hymenoptera, Apidae (bees); (e) Diptera,
Ceratopogonidae (biting midges); (f) Diptera, Glossinidae (tsetse flies).
ECTOGNATHOUS MOUTHPARTS 17
mandible
mandible
food
canal
groove groove
mandible
lacinea
food mandible
mandible food mandible canal
canal
groove
food
canal
groove
lacinea
Fig. 2.5. Sucking mouthparts of larval holometabolous insects. (a) An antlion (Neuroptera); (b) Dytiscus larva (Coleoptera,
Dytiscidae); (c) a firefly larva (Coleoptera, Lampyridae). Arrows show the positions at which the food canal opens to the
outside (based on Cicero, 1994).
lobe, the labellum which, in Brachycera, is traversed by a elongation and flattening of the galeae and labial palps
series of grooves known as pseudotracheae because they which surround the fused glossae (Fig. 2.4d). The space
are held open by cuticular ribs giving them a superficial outside the glossal tongue forms the food canal. The sali-
similarity to tracheae. The pseudotracheae converge cen- vary canal is in the posterior folds of the tongue.
trally on the distal end of the food canal. Diptera have Larval Neuroptera and some predaceous larval
maxillary palps, but no labial palps. Coleoptera that digest their prey extra-orally have a food
The food canal of fleas is formed between an extension canal in each of the mandibles. These function in a similar
of the epipharynx and the maxillary stylets (Fig. 2.4b). A way to those of biting and chewing insects, but they are
salivary canal extends along the inside of each maxilla sickle-shaped. In larval Neuroptera, a groove on the inside
which also form the piercing organs. Both maxillary and of each mandible is converted to a tube by the juxtaposi-
labial palps are present. tion of a slender lacinea (Fig. 2.5a). A similar groove is
The proboscis of adult Lepidoptera is formed from the present in the mandibles of some larval Dytiscidae, but
galeae held together by a system of cuticular hooks ven- instead of being closed by the lacinea the lips of the groove
trally and a series of plates dorsally (Fig. 2.4c). Since most almost join to form a tube (Fig. 2.5b). Larval Lampyridae
Lepidoptera are nectar feeders, they do not require pierc- have a tube running through each mandible and opening
ing mechanisms and the rest of the mouthparts, apart from by a hole near the tip and another near the base within the
the labial palps, are reduced or absent. There is no salivary cibarial cavity (Fig. 2.5c) (Cicero, 1994).
canal although adult Lepidoptera do have salivary glands. Associated with the production of a tube for feeding is
Adults of most Hymenoptera have biting and chewing the development of a pump for drawing up the fluids and a
mouthparts, but the bees are nectar-feeders and are salivary pump for injecting saliva (see Fig. 3.15). Often the
described as lapping the nectar. This is achieved by an feeding pump is developed from the cibarium, which by
18 MOUTHPARTS AND FEEDING
extension of the lateral lips of the mouth becomes a closed teeth to rasp through the tissues, such as Glossina and
chamber connecting with the food canal. The cibarial Stomoxys, however, the labial sensilla come into direct
muscles from the clypeus enlarge so that a powerful pump contact with the blood. This is also true of nectar feeding
is produced. In Lepidoptera and Hymenoptera the cibarial insects, Lepidoptera, Apoidea and many Diptera, includ-
pump is combined with a pharyngeal pump which has ing female mosquitoes. Cibarial sensilla are known to be
dilators arising on the frons. present in some of these species and are probably uni-
Review: Smith, 1985 versal.
The axons of contact chemoreceptors and mechanore-
2.1.4 Sensilla on the mouthparts ceptors on the mandibles, maxillae and labium end in
Most of the sensilla on the mouthparts are contact chemo- arborizations in the corresponding neuromeres of the sub-
receptors, but mechanoreceptors are also common and esophageal ganglion, but the axons from olfactory sensilla
olfactory sensilla are often present on the palps. on the palps run directly to the olfactory lobes. The axons
Chordotonal organs, that probably function as pressure of sensilla on the labrum arborize in the tritocerebrum.
receptors, are present at the tips of the mandibular cusps Interneurons responding to chemical and mechanical
and also in the lacinea where this is heavily sclerotized and stimulation of the mouthpart receptors have been demon-
tooth-like. strated in the subesophageal ganglion of Sarcophaga
Biting and chewing insects have contact chemo- (Mitchell & Itagaki, 1992) and must presumably occur in
receptors on all the mouthparts except the mandibles. all insects with functional mouthparts. The cell bodies of
They also have chemoreceptors on the dorsal and ventral the motor neurons regulating movements of the mouth-
walls of the cibarium, often called epipharyngeal and parts are also present in this ganglion, but nothing is
hypopharyngeal sensilla, respectively. Orthoptera and known of the precise pathways that connect the sensory
Blattodea have large numbers of sensilla in groups (Fig. and motor systems.
2.6a) with especially large numbers on the tips of the max- Reviews: Backus, 1988 – plant-feeding Hemiptera; Chapman,
illary and labial palps. Gryllus bimaculatus, for example, 1982 – all insect groups
has over 3000 sensilla on each maxillary palp. Because each
sensillum contains at least four neurons, the potential
2.2 MECHANICS AND CONTROL OF FEEDING
chemosensory input to the central nervous system is
considerable; an adult locust has about 16 000 chemo- Before an insect starts to feed it exhibits a series of behav-
sensory neurons on the mouthparts. In the orthopteroid ioral activities which may lead to acceptance or rejection of
insects, the numbers increase each time the insect molts. the food. A grasshopper first touches the surface of the
By contrast, caterpillars have only about 100 neurons in plant with the sensilla at the tips of its palps. This behavior
mouthpart receptors and the closely associated antennae enables the insect to monitor the chemicals on the surface
(Fig. 2.6b); the number does not increase during larval life. of the plant wax and perhaps also the odor of the plant.
Fluid-feeding insects usually have chemoreceptors at the This may lead the insect to reject the plant without further
tip of the labium, on the palps when these are present, and investigation or to make an exploratory bite, presumably
in the walls of the cibarium (Fig. 2.6c). In addition, at least releasing chemicals from within the plant. This, in turn,
some planthoppers have an olfactory sensillum towards may result in rejection, or the insect may start to feed.
the tip of the rostrum. No chemoreceptors are present on Essentially similar behaviors are seen in caterpillars and
the mandibular and maxillary stylets. Aphids have only leaf-eating beetles.
mechanoreceptors at the tip of the labium; their only The principal chemicals inducing feeding (phagostimu-
chemoreceptors on the mouthparts are in the cibarium. lants) of leaf-eating insects are sucrose and hexose sugars,
In piercing and sucking insects (Hemiptera and but the exploratory bite following palpation may be induced
Culicidae, for example) only the cibarial sensilla come by components of the leaf wax. Insects that feed only on
directly into contact with the food as it is ingested; the specific plant taxa may require the presence of a compound
labium does not enter the tissues of the host so that its sen- that is characteristic of the plant species, or group of
silla can only monitor the outer surface of the food, either species. For example, many caterpillars and beetles that feed
plant or animal. In blood-sucking species that use labial on plants in the family Brassicaceae, which includes
MECHANICS AND CONTROL OF FEEDING 19
Fig. 2.6. Chemoreceptors on the mouthparts of various insects. Numbers show the number of sensilla and, in brackets, the
number of chemosensitive neurons in each group of receptors. Sensilla are contact chemoreceptors unless otherwise stated.
The numbers do not include sensilla scattered over the mouthparts, which may be present in addition to those in groups. (a)
An adult locust, Locusta; (b) a caterpillar, Pieris; (c) an adult fly, Drosophila.
cabbage, are stimulated to feed by mustard oil glucosides feeding, known as feeding deterrents (see section 24.2.2).
(glucosinolates) that are characteristic of this plant family. Information from all the sensilla is integrated in the central
Some species with restricted host ranges have chemo- nervous system. Whether or not the insect feeds depends on
sensory neurons in the mouthpart sensilla which respond the balance between phagostimulants and deterrents.
specifically to the indicator chemicals. Other neurons are Amongst nectar-feeding insects, sugars are phagostim-
sensitive to sugars, and others to compounds that inhibit ulants. Before starting to feed, the insects exhibit a
20 MOUTHPARTS AND FEEDING
sequence of behaviors comparable with that of the leaf- stimulation of the labrum. Sensilla which detect the posi-
chewing insects. If the tarsi contact sugar above a certain tions of the open mandibles then stimulate the mandibular
threshold concentration, the proboscis is extended. This is adductor muscle motor neurons via the ganglion so that
true of flies, bees and butterflies. Stimulation of the tri- the mandibles close. This stimulates other receptors, prob-
choid sensilla on the outside of the labellum of a fly causes ably those at the tips of the cusps, which presumably starts
the insect to spread the labellar lobes so that the inter- another cycle of opening.
pseudotracheal papillae (see Fig. 2.6c) contact the food. A modulatory effect on the activity of the muscles of
Their stimulation initiates ingestion. When female blood- the mouthparts is probably exerted by serotonin. In the
sucking insects, such as mosquitoes, feed on nectar the cockroach, Periplaneta, and some other insects all the
stylets remain enclosed in the labium and the labellar nerves to these muscles have a branching network of fine
chemoreceptors are stimulated. serotonergic axons over their surfaces. These neurons of
Blood-sucking insects fall into two classes with respect which the axons are a part are only active during feeding
to the factors regulating ingestion: those that will gorge on and it is presumed that the electrical activity leads to the
saline solutions which are isotonic with vertebrate blood, release of serotonin from the fine branches where they
and those that require the presence of an adenine nucleo- locally affect the activity of the muscles moving the mouth-
tide. Amongst the former are sandflies (Ceratopogonidae), parts (Schachtner & Bräunig, 1993). The precise effect of
anopheline mosquitoes and fleas, although fleas require the this modulation is not known.
presence of a nucleotide to take a full meal. Most of the Review: Chapman, 1995
other blood-suckers require a nucleotide. ATP is generally
much more stimulating than ADP, and this in turn is much 2.2.2 Fluid-feeding insects
more effective than AMP. ATP is normally contained Proboscis extension by nectar-feeding flies and bees
within red blood cells where it would not stimulate the depends on the activity of muscles associated with the
insect’s sensory neurons. It is released by damage to these mouthparts (Rehder, 1989). In Lepidoptera, the proboscis
cells during probing, but is quickly degraded by the is caused to unroll by increased pressure of the hemo-
insect’s own salivary apyrase. lymph. This pressure is generated in the stipes associated
Reviews: Bernays & Chapman, 1994 – phytophagous insects; with each galea. A valve isolates the hemocoel of the stipes
Davis & Friend, 1995 – blood-feeding insects when the latter contracts. Coiling results from the elastic-
ity of the cuticle of the galeae together with the activity of
2.2.1 Biting and chewing insects intrinsic muscles (Krenn, 1990).
Biting and chewing insects make regular opening and Insects feeding on the internal fluids of other organ-
closing movements of the mandibles; both locusts and isms must first penetrate the host tissues. Homoptera,
caterpillars commonly make up to four bites per second which feed on plants, first secrete a blob of viscous saliva
when feeding continuously, but the rate probably varies which solidifies around the labellar lobes forming a sali-
with temperature, the quality of the food, and the feeding vary flange which remains even after the insect has left
state of the insect. As a result of a sequence of bites, the (Fig. 2.7). This probably serves to prevent the stylets from
insect cuts off a fragment of food which is pushed back slipping over the plant surface as pressure is applied. The
towards the mouth by the mandibles, often aided by the mandibles penetrate the leaf cuticle and epidermis; sub-
maxillae. Periods of continuous biting are often separated sequent deeper penetration may involve the maxillae
by short pauses, presumably associated with swallowing alone, or both maxillae and mandibles. The stylets of
the food. The pauses get longer as a meal progresses. aphids and other small Homoptera move within the walls
The motor pattern controlling movement of the of the plant cells aided by enzymes in the watery saliva (see
mouthparts is generated in the subesophageal ganglion. In section 2.5). As the stylets progress through the leaf, the
caterpillars of Manduca, chewing activity occurs insect secretes more of the viscous saliva that solidifies to
spontaneously in the absence of input from receptors in form a sheath around them (Fig. 2.8a). The significance of
the wall of the thoracic segments, but in grasshoppers such this sheath is not known. It may serve to support the stylets
spontaneous activity does not occur. The mandibular and to prevent loss of plant sap and of the more fluid saliva
abductor muscles are stimulated to contract by mechanical through the wound in the epidermis. The stylets often
MECHANICS AND CONTROL OF FEEDING 21
break out of the plant cell wall, and, when they do, the vertebrates, the proboscis is moved into the feeding posi-
insect is believed to sample the chemical composition of tion in response to the warmth of the host. In mosquitoes
the fluid by drawing it up to the cibarial sensilla. If the and triatomine bugs, the stylets are pushed into the tissues
stylets are not in a sieve element of the phloem, the insect and the labium folds up, but does not enter the wound.
withdraws its stylets for a short distance and moves them This separation of the stylets from the ensheathing labium
in another direction. This process is repeated, and the path appears to provide some additional stimulus necessary for
of the stylets may become very irregular (Fig. 2.8b), until the insects to take a full blood meal. In tsetse and stable
the phloem is entered, then the stylets are pushed into it flies, rasping movements of the prestomal (labial) teeth
and ingestion begins (Fig. 2.8b) (Tjallingii & Esch, 1993). tear into the tissues. Blood vessels comprise less than 5%
It may take anything from five minutes to three hours from of the volume of mammalian skin so that blood is not avail-
the beginning of probing until a feeding site is reached. In able until a vessel is ruptured.
larger Homoptera, stylet entry occurs in a similar way and Salivary secretions play a critical role in blocking the
a salivary sheath is formed, but in most cases the stylet hemostatic responses of the host which tend to prevent
pathway is through cells rather then between them. blood loss. Three different processes contribute to hemo-
Blood-sucking insects, like the Homoptera amongst stasis: platelet aggregation, blood coagulation and vaso-
plant-feeders, must penetrate the host tissues before start- constriction. The saliva of blood-sucking insects contains
ing to feed. In many species that feed on warm-blooded chemicals that inhibit all three (Table 2.1). ADP released
22 MOUTHPARTS AND FEEDING
Table 2.1. Components of saliva of blood-sucking insects that inhibit the hemostatic responses of their vertebrate hosts
Inhibiting
platelet
Insect Order Family aggregation Vasodilator Anticoagulant
Notes:
? No compound known.
a Enzyme.
b Peptide.
c Factor VII and factor X are substances involved in normal blood clotting.
from injured blood cells is an important signal for platelet are consequently different in insects with different feeding
aggregation and blood-sucking insects generally have a habits. Capillarity may be important in bees, helping to
salivary apyrase that degrades ADP to orthophosphate and move nectar up the food canal.
AMP. The saliva also contains a vasodilator to counteract Once a phloem feeding insect, such as an aphid or plan-
the vasoconstriction induced by the host, but these thopper, has reached the phloem, the pressure of the
vasodilators differ from one insect species to another. phloem is sufficient to push fluid into the insect, which
Factor X and thrombin are chemicals that regulate appears then to play no active role in ingestion. These
coagulation; peptides that counteract the effects of both insects can, however, pump fluid into the gut when the
chemicals are present in the saliva. food is not under pressure and do, periodically, feed from
The intake of fluids depends on their viscosity and parenchyma or xylem.
whether or not they are under pressure. Viscosity increases The negative pressure of xylem tends to draw fluid out
with the concentration of dissolved solutes so that nectar of the insect, and the massive cibarial pumps that are
containing 40% sucrose is six times more viscous than water characteristic of habitual xylem-feeding insects, such as
at the same temperature. The phloem and xylem of plants cicadas and cercopids, are necessary to overcome these
are very dilute so their viscosities are not markedly different pressures (Fig. 3.15). Even so, the leafhopper,
from water. The viscosity of vertebrate blood, however, Homalodisca, exhibits markedly reduced feeding rates at
varies with the diameter of the tube through which it is negative xylem pressures in excess of ⫺1.5 MPa
being drawn. For tubes less than 100 m in diameter, the (Andersen, Brodeck & Mizell, 1992).
viscosity falls as tube diameter is reduced down to about In nectar-feeding bees, the glossa is repeatedly
6 m. At smaller diameters it increases sharply because flow extended into the nectar while the galeae and labial palps
depends on the distortion of the red blood cells. In addition, which surround it (Fig. 2.4d) remain motionless. During
the fluid may be under positive or negative pressure. Blood extension of the glossa nectar moves on to it by capillarity.
pressure in human capillaries is about 3 kPa, whereas the The fluid moves the hairs on the glossa to a position at
phloem in plants is under much higher pressure, 0.2 to right angle to the surface of the glossa so that the volume of
1 MPa. Xylem, on the other hand, is under strong negative fluid that is held is increased. When the glossa is retracted
pressure, as much as ⫺2 MPa and higher. The cibarial and into the tube formed by the galeae and labial palps the fluid
pharyngeal pumps which draw fluid through the proboscis is drawn into the cibarium by the pump. In Bombus these
24 MOUTHPARTS AND FEEDING
licking movements occur at a frequency of about 5 Hz. a position on either side of the head. The attack involves
The intake rate of sucrose solutions at concentrations up the strike by the forelegs and a forwards lunge of the whole
to about 40% is around 1.75 l s⫺1. It declines at higher body that reduces the distance between the head of the
concentrations due to the increasing viscosity. mantid and its prey. The strike involves first the extension
Blood-sucking insects produce pressure differentials of the coxa and tibia and then a rapid extension of the
well in excess of the capillary blood pressure of the host, so femur and flexure of the tibia to grasp the prey. This last
the latter is unlikely to play a significant role in feeding. movement occurs in about 30 ms (Corrette, 1990; Rossel,
Calculated pressure differences, which are produced by 1991).
the cibarial and pharyngeal pumps, are approximately Dragonfly larvae also sit and wait for their prey and
8 kPa in the mosquito, Aedes, 20 kPa in the louse, Pediculus, then capture it with the modified labium. The post-
80 kPa in the bedbug, Cimex, and 100–200 kPa in Rhodnius. mentum and prementum are both elongate and the labial
In the latter, the pumping rate is about 7 Hz producing an palps are claw-like structures set distally on the pre-
ingestion rate of about 450 nl s⫺1. In the mosquito, Aedes, mentum (Fig. 2.10a). At rest, the labium, often referred to
the intake rate is about 16 nl s⫺1. The louse, Pediculus, has as a labial mask, is folded beneath the head. If a potential
a food canal that is smaller than the diameter of a human prey item comes within range, the mask is extended and
red blood cell (about 7.5 m). As a result, the feeding rate the prey caught by the labial palps (Fig. 2.10c). As in the
of an adult female louse is about five times lower than in mantis, the strike is very rapid, being completed in 25 ms
the mosquito. or less, but in this case the speed of the strike depends on
Little is known about the control of feeding in fluid- prior energy storage (see section 8.4.2). Before the strike,
feeding insects, but serotonin is released into the hemo- the anal sphincter is closed and the dorsoventral abdomi-
lymph during feeding by Rhodnius probably from nal muscles contract (Fig. 2.10b). This results in an
neurohemal organs on the abdominal nerves. It triggers increase in hemolymph pressure. At the same time the
plasticization of the abdominal cuticle (section 16.3.3) flexor and extensor muscles of the prementum, which
(Lange, Orchard & Barrett, 1989). arise in the head, contract together (co-contract) so that
Review: Kingsolver & Daniel, 1995 the labial mask is held against the head and, presumably,
tension builds up at the postmentum/prementum joint.
2.2.3 Prey capture by predaceous insects Relaxation of the flexor muscle results in the sudden
Predators catch their prey either by sitting and waiting for extension of the prementum due to the continued activity
it to come their way, or by actively pursuing it. The mantis of the premental extensor muscles and release of the cut-
is an example of an insect that sits and waits. Like many icular tension at the postmentum/prementum joint.
predators, mantids have wide heads so that the eyes are rel- There are no extensor muscles of the postmentum and its
atively far apart. This facilitates the accurate determina- extension is produced by the high hemolymph pressure
tion of the distance of the prey from the insect (see Fig. (Parry, 1983; Tanaka & Hisada, 1980).
22.17). In addition, the head is very mobile so that move- Some insects that sit and wait for prey construct traps.
ments of the prey can be followed without the whole Antlions (larval Myrmeleontidae), for instance, dig pits
mantis moving. The mantis strikes when the prey is of a two to five centimeters in diameter with sloping sides in
suitable size, is at a suitable distance in front of the head, dry sand. The insect then buries itself in the sand at the
and is moving. Sphodromantis, a relatively large insect, bottom of the pit with only the head exposed. If an ant
strikes when the prey subtends an angle of 20–40 ° at the walks over the edge of such a pit it has difficulty regaining
eyes and is 30 to 40 mm in front of the head. In Tenodera the top because of the instability of the sides. In addition,
the attack zone is in an area defined by the length of the the larva, by sharp movements of the head, flicks sand at
foreleg and below the body axis (Fig. 2.9). The forelegs of the ant causing it to fall to the bottom of the pit and be cap-
mantids are raptorial and armed with spines. The mantis tured.
follows the prey with its eyes (see Fig. 22.18) and moves its Larvae of the fly, Arachnocampa (Mycetophilidae), are
prothorax to orient directly at the prey. The effect of this is luminescent and use the light to lure prey into a sticky trap
to make the area of attack two dimensional; the mantis has consisting of vertical threads of silk studded with sticky
to judge the position of the prey directly in front and not to drops.
MECHANICS AND CONTROL OF FEEDING 25
Fig. 2.9. Prey capture by a mantis, Tenodera (after Corrette, 1990). (a) Area of capture relative to the head. The vertically
hatched area shows the region in which prey can be captured by striking with the forelegs without any other movement of the
body. (b) Area of capture made possible by changes in orientation coupled with the lunge, shown by oblique hatching. Before
the lunge, the insect may occupy any position between the two extremes shown in the diagram. (c) Diagrams of the changes in
position associated with capturing prey. 0 ms, start of strike; 30 ms, start of lunge; 70 ms, capture. The vertical line is a
reference showing the forward movement of the body during the lunge. The black spot represents the position of the target.
(d) Changes in the angles between leg segments (shown in a) at times corresponding with the positions shown in (c). Notice
the rapid increase in  (extension of the femur) coincident with the decrease in ␥ (flexion of the tibia to grasp the prey).
Adult dragonflies are active aerial hunters, pursuing it encounters prey they snap shut in less than 1 ms. Such a
other insects in flight. Their thoracic segments are rotated rapid closure could not be achieved by direct muscular
forwards ventrally bringing the legs into an anterior posi- action, and it is probable that there is some method of devel-
tion which facilitates grasping (Fig. 2.11). Tiger beetles oping tension at the mandibular articulation with the head
(Coleoptera, Cicindelidae) hunt on the ground and have analogous to that found in jumping mechanisms (section
long legs, which enable them to move quickly, and prog- 8.4.2) (Gronenberg, Tautz & Hölldobler, 1993).
nathous mouthparts with large mandibles. In the trap jaw These active hunters have well-developed eyes since
ant, Odontomachus, mandible closure is triggered by only vision can give a sufficiently rapid directed response
mechanical stimulation of a hair on the inside of the to moving prey. The visual response is usually not specific
mandible. This ant hunts with its jaws wide open, and when and the predator will pursue any moving object of suitable
26 MOUTHPARTS AND FEEDING
Fig. 2.10. Strike of a dragonfly larva (partly after Tanaka & Hisada, 1980). (a) Dorsal view of an extended labial mask with its principal
muscles. (b) Timing of activity of the muscles relative to the strike. (c) Lateral view showing the labial mask retracted and extended. (d)
Changes in the angles between the prementum and postmentum (angle ␣) and the postmentum and prothorax (angle ) during the strike.
The positions of the angles are shown in (c).
size. Thus a dragonfly will turn towards a small stone Many Hymenoptera use a sting to inject venom into
thrown into the air, and the wasp, Philanthus, orients to a their prey (see section 27.2.7). Amongst predaceous
variety of moving objects, although it only catches objects Heteroptera, the prey is rapidly subdued, apparently by
having the smell of bees. fast-acting lytic processes caused by enzymes from the
Mechanical stimulation is sometimes important in salivary glands or midgut rather than by specific toxins.
finding prey. Notonecta is able to locate prey trapped in the
air/water interface as a result of the ripples which radiate
2.3 REGULATION OF FEEDING
from the struggling object. The vibrations are perceived
by mechanoreceptors on the swimming legs. Coccinellid Most insects eat discrete meals separated by relatively long
larvae preying on aphids only respond to the prey on periods of non-feeding (Fig. 2.12, Table 2.2). A meal may
contact. weigh more than 10% of the body weight, and in some
REGULATION OF FEEDING 27
a) food
time since last present
meal
absent
0.1
tendency to start
light
on
feeding
0.01 off
0 60 120
min
defecation
Fig. 2.11. Diagram of a male dragonfly to show the oblique 0.001 short-term rhythm
development of the thorax bringing the legs into an anterior
position, which facilitates grasping the prey.
15 min 30 min
a) Manduca
b)
0 1 2 3 4
time (hours)
Meal size
Time
Insect (% body Meal duration Time between feeding
Insect Order Food weight (mg) (mg) weight) (min) meals %
Locusta (larva) Orthoptera Leaves 2700 118 17 226–8 270–80 min 227–11
Nilaparvata (female) Hemiptera Plant fluids 2222.5 — — Continuous — 285
Zelus (female) Hemiptera Insect contents 2105 ⬃20 ⬃20 130 ⬎24 h ⬍9
Rhodnius (larva) Hemiptera Vertebrate blood 2240 300 750 215 days ⬍1
Manduca (larva) Lepidoptera Leaves 3500 280 222 210–25 215–25 min 225–60
Vanessa (adult) Lepidoptera Nectar 2600 230 225 221 130 min 214a
Lucilia (adult) Diptera Nectar 2225 222 8 220.5–1 225–40 min 221–3.5b
Apis (adult,worker) Hymenoptera Nectar 2290 230 33 230–80c — 48c
Apis (adult,worker) Hymenoptera Pollen 2290 220 22 210c — 12c
Notes:
a Feeding on flowers in the laboratory. Used for energy supply; in other insects listed food is for
b Feeding on glucose solution. 其 growth and/or egg development, as well as energy.
c Foraging on flowers in the field. Includes foraging time.
REGULATION OF FEEDING 29
especially important in social Hymenoptera where they over 30% of royal jelly; the food of worker larvae has, at
are important sources of pheromones (see section 27.1.1 first, only about 12% sugar. Consequently, queen larvae
and Fig. 27.3). eat much more food and grow bigger. Worker bees feed
Hypopharyngeal glands occur in Hymenoptera and are either type of larva, apparently regulating the food they
particularly well developed in worker honeybees. They are give according to the type of larva they visit. The conse-
vestigial in queens and absent from males. There is one quences of the differences in food on larval development
gland on each side of the head consisting of a long coiled are discussed in section 15.5.
duct with numerous small glandular lobes attached to it. Maxillary glands are found in Protura, Collembola,
The ducts open at the base of the hypopharynx. These Heteroptera and some larval Neuroptera and
glands produce an invertase as well as components of Hymenoptera. They are usually small, opening near the
brood food. bases of the maxillae, and may be concerned with lubrica-
Secretions from the hypopharyngeal and mandibular tion of the mouthparts.
glands of worker honeybees are fed to larvae and regulate
their development into queen or worker bees. Queen 2.5.2 Labial glands
larvae receive mainly the secretion of the mandibular The most commonly occurring head glands are the labial
glands during their first three days of development, then, glands which are present in all the major orders of insects
for the last two days, their food contains roughly equal except the Coleoptera. In most insects they function as
amounts of secretion from the two glands. Worker larvae, salivary glands.
by contrast receive a much greater proportion of the nutri-
ent from the hypopharyngeal glands. The ‘royal jelly’ on 2.5.2.1 Structure
which queen larvae are fed contains many different com- The labial glands of most insects are acinous glands (Fig.
pounds including large amounts of 10-hydroxy-trans-2- 2.16), but in Lepidoptera, Diptera and Siphonaptera (fleas)
decanoic acid, nucleic acids, and all the common amino they are tubular with the ducts swelling to form the terminal
acids. It also contains about 10 times more pantothenic glandular parts (Fig. 2.17). Sometimes, as in cockroaches,
acid (a B vitamin) and biopterin than food fed to worker there is also a salivary reservoir, while in Heteroptera the
larvae. Sugars, which act as phagostimulants, comprise gland consists of a number of separate lobes (Fig. 2.18).
Fig. 2.16. Acinous salivary gland. Open arrows show the movement of sodium and water; black arrows show the movements
of enzymes. (a) General arrangement in Locusta. (b) Section through an acinus of Nauphoeta (after Maxwell, 1978).
(c) Section through a duct cell of Schistocerca (after Kendall, 1969).
32 MOUTHPARTS AND FEEDING
Fig. 2.17. Tubular salivary gland of Calliphora. At the top is a representation of the gland showing the positions of the cells
depicted below. Left: secretory cell; center: cuboid cell; right: duct cell. Open arrows show the movement of potassium and
water; black arrows show the movements of enzymes (after Oschman & Berridge, 1970).
lateral lobe reticulum and Golgi bodies and probably produce the
enzymes. The peripheral, or parietal, cells have an exten-
posterior anterior
lobe lobe sive microvillar border to the channel leading to the lumen
of the duct. These cells are responsible for the movement
accessory salivary
gland duct of water into the lumen of the gland. In tubular glands
both functions appear to be performed by the same cells.
The movement of water results from the creation of an
osmotic gradient across the cells by H⫹-ATPase pumps in
the microvillar plasma membrane. The pumps move
Fig. 2.18. Salivary glands of a hemipteran showing the different protons into the lumen, and the protons are then
lobes (Oncopeltus) (after Miles, 1960).
exchanged for sodium or potassium at cation/H⫹ anti-
porters resulting in a high ionic concentration in the
The cells of the gland and duct are differentiated to lumen. The duct cells of acinous glands, or the cuboid cells
perform three functions: the production and secretion of of tubular glands, remove cations from the salivary secre-
enzymes and other chemicals present in the saliva, move- tion, and those of the cockroach have sodium/potassium
ment of water from the hemolymph into the lumen by the pumps in the basal plasma membrane (Just & Walz, 1994).
active secretion of sodium or potassium, and modification The ducts from the glands run forwards and unite to
of the fluid as it passes down the salivary duct by resorp- form a single median duct which opens just behind or on
tion of ions and, perhaps, some water. In acinous glands, the hypopharynx. In fluid-feeding insects, muscles in the
the central, or zymogen, cells have extensive endoplasmic head insert on to the duct to form a salivary pump. At this
HEAD GLANDS 33
point the lower wall of the duct is rigid while the upper enzymes, but it does have components to overcome the
part is flexible. It is pulled up by the dilator muscles so that hemostatic responses of the host (Table 2.1). In a number
fluid is drawn into the lumen of the pump. There are no of insects, specific enzymes are present in the saliva that
compressor muscles. When the dilators relax, the upper facilitate penetration and digestion of the food (Table 2.3).
wall springs down by virtue of the elasticity of the cuticle For example, leaf cutting ants, Acromyrmex, have a salivary
lining the pump and forces saliva out. In some insects, at chitinase that attacks chitin in the fungus on which the
least, valves ensure the forward flow of saliva. insects feed; larval warble flies, Hypoderma, that bore in
the subcutaneous tissues of cattle, secrete a collagenase
2.5.2.2 Control of secretion which facilitates movement of the larva through the tissues
Acinous glands are innervated by axons from the sub- of the host.
esophageal ganglion and from the stomatogastric system. Plant-sucking Hemiptera produce two types of saliva, a
In both cockroach and locust, one of the innervating typical watery saliva carrying enzymes, and another which
neurons produces dopamine, another serotonin. hardens to form the salivary sheath (Fig. 2.8). The enzymes
Dopamine stimulates the secretion of fluid, while sero- in watery saliva are produced in the posterior lobe of the
tonin causes the central cells to produce and secrete the glands and water probably comes from the accessory gland.
enzymes (Just & Walz, 1996). In addition, a network of The watery saliva is produced during penetration of the
branches of an octopaminergic neuron is closely associated plant tissues and some of its enzymes facilitate penetration
with the salivary glands of Locusta. through the middle lamellae of plant cell walls. Aphids, for
Tubular glands are not directly innervated although in example, have both a pectinesterase and a galacturonidase.
the female mosquito, Aedes aegypti, a plexus of nerves In addition, the saliva in some species contains an amylase
closely surrounds part of the gland. In both Aedes and and a proteinase which contribute to extra-oral digestion of
Calliphora, serotonin, acting directly on the gland, regu- the plant tissue. Amino acids may be present in relatively
lates the production and release of saliva. In Aedes, the large amounts in the saliva (Laurema & Varis, 1991) and it is
serotonin is released from the neural plexus adjacent to the possible that the aphids excrete unutilized dietary compo-
gland, while in Calliphora it comes from neurohemal nents in this way. The sheath material comes from the ante-
organs on the ventral nerves in the abdomen. rior and lateral lobes of the gland in the milkweed bug,
The production of saliva results from stimulation of Oncopeltus. It contains a catechol oxidase and a peroxidase
chemoreceptors on the mouthparts; in Calliphora, which perhaps counter the effects of products produced by
stimulation of the interpseudotracheal pegs is necessary. plants to inhibit insect feeding (Miles & Earthly, 1993).
In most insects, production and release occur together, but Male scorpion flies (Mecoptera) have enlarged salivary
in insects with a salivary reservoir the two processes may glands and produce large quantities of saliva which are
be separately controlled. Production stops when sensory eaten by the female during copulation.
input is removed. In Calliphora it takes less than two
minutes to clear the serotonin from the hemolymph when Trophallaxis Many species of wasps and ants, and some
feeding stops and the interpseudotracheal pegs are no bees, exchange fluids with larvae. The larvae of these
longer stimulated. species have enlarged salivary glands (Fig. 2.19) which
Reviews: Ali, 1997 – innervation; House & Ginsborg, 1985 – appear to be the source of the fluids they regurgitate.
pharmacology Larvae of vespid wasps produce saliva containing sugars at
concentrations of 10 mg ml⫺1 or more, principally glucose
2.5.2.3 Functions of saliva and trehalose, about 1% proteins and 18–24 amino acids at
Saliva serves to lubricate the mouthparts and more is pro- total concentrations ranging from 25 to 95 mol l⫺1 (Abe
duced if the food is dry. It also contains enzymes which et al., 1991). Larval ants produce salivary secretions from
start digestion of the food. The presence of particular which carbohydrates are absent, but which contain high
enzymes is related to diet, but an amylase, converting concentrations of amino acids and proteins, including a
starch to sugar, and an invertase, converting sucrose to number of enzymes. These enzymes may add to the
glucose and fructose, are commonly present (Table 2.3). In amounts present in the midguts of adult ants, although
blood-sucking insects, the saliva contains no digestive the significance of the transfer is unclear. The nutrient
34 MOUTHPARTS AND FEEDING
Enzymes
Notes:
⫹, present; ⫺, absent; ⫾, present in some species, not others; ?, not known.
a Digests components of plant cell walls.
b Digests insect connective tissue.
c Digests vertebrate collagen.
d Digests chitin in fungi.
36 MOUTHPARTS AND FEEDING
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Kawasaki, Y.Y. (1991). Comparative look at thrips (Thysanoptera) mouth- serotonin and dopamine on salivary
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Biochemistry and Physiology, 99C, Cicero, J.M. (1994). Composite, haustel- Kendall, M.D. (1969). The fine structure
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Biology, 200, 1941–9. Corrette, B.J. (1990). Prey capture in the 399–420.
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R.F. (1992). Feeding by the leaf hopper, sinensis: coordination of the capture Mechanics of food handling by fluid-
Homalodisca coagulata, in relation to sequence and strike movements. feeding insects. In Regulatory
xylem fluid chemistry and tension. Journal of Experimental Biology, 148, Mechanisms in Insect Feeding, ed.
Journal of Insect Physiology, 38, 147–80. R.F.Chapman & G.de Boer, pp. 157–89.
611–22. Davis, E.E. & Friend, W.G. (1995). New York: Chapman & Hall.
Backus, E.A. (1988). Sensory systems and Regulation of a meal: blood feeders. In Krenn, H.W. (1990). Functional mor-
behaviours which mediate hemipteran Regulatory Mechanisms in Insect phology and movements of the pro-
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Host-plant Selection by Phytophagous Denis, R. (1949). Sous-classe des (1989). Changes in the hemolymph
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Bernays, E.A. & Simpson, S.J. (1982). 9, ed. P.-P.Grassé, pp. 111–275. Paris: in the blood-sucking bug, Rhodnius pro-
Control of food intake. Advances in Masson et Cie. lixus. Journal of Insect Physiology, 35,
Insect Physiology, 16, 59–118. Gronenberg, W., Tautz, J. & Hölldobler, 393–9.
Blaney, W.M., Chapman, R.F. & Wilson, B. (1993). Fast trap jaws and giant Laurema, S. & Varis, A.-L. (1991).
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Chapman, R.F. (1982). Chemoreception: Ants. Cambridge, Mass: Harvard Maschwitz, U. (1966). Das Speichelsekret
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Advances in Insect Physiology, 16, House, C.R. & Ginsborg, B.L. (1985). logische Bedeutung. Zeitschrift für
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Regulatory Mechanisms in Insect & L.I.Gilbert, pp. 195–224. Oxford: axons associated with the salivary appa-
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pp. 3–31. New York: Chapman & Hall. Hunt, J.A. & Nalepa, C.A. (ed.) (1994). cinerea. Tissue & Cell, 10, 699–706.
Chapman, R.F. & Beerling, E.A.M. Nourishment and Evolution in Insect Miles, P.W. (1960). The salivary secretions
(1990). The pattern of feeding of first Societies. Boulder, Colorado: Westview of a plant-sucking bug, Oncopeltus fas-
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Regulatory Mechanisms in Insect in the salivary glands of the cockroach, Miles, P.W. (1972). The saliva of
Feeding. New York: Chapman & Periplaneta americana. Cell and Tissue Hemiptera. Advances in Insect
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Miles, P.W. & Earthly, J.J. (1993). The Reynolds, S.E., Yeomans, M.R. & Snodgrass, R.E. (1935). Principles of
significance of antioxidants in the Timmins, W.A. (1986). The feeding Insect Morphology. New York:
aphid-plant interaction: the redox behaviour of caterpillars (Manduca McGraw-Hill.
hypothesis. Entomologia Experimentalis sexta) on tobacco and on artificial diet. Snodgrass, R.E. (1944). The feeding
et Applicata, 67, 275–83. Physiological Entomology, 11, 39–51. apparatus of biting and sucking insects
Mitchell, B.K. & Itagaki, H. (1992). Ribeiro, J.M.C. (1995). Insect saliva: func- affecting man and animals. Smithsonian
Interneurons of the subesophageal gan- tion, biochemistry and physiology. In Miscellaneous Collections, 107, no. 7,
glion of Sarcophaga bullata responding Regulatory Mechanisms in Insect 113 pp.
to gustatory and mechanosensory Feeding, ed. R.F.Chapman & G.de Tanaka, Y. & Hisada, M. (1980). The
stimuli. Journal of Comparative Boer, pp. 74–97. New York: Chapman hydraulic mechanism of the predatory
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Nakamuta, K. (1985). Mechanism of the Rossel, S. (1991). Spatial vision in the Experimental Biology, 88, 1–19.
switchover from extensive to area-con- preying mantis: is distance implicated Tjallingii, W.F. (1995). Regulation of
centrated search behaviour of the lady- in size detection? Journal of phloem sap feeding by aphids. In
beetle, Coccinella septempunctata bruckii. Comparative Physiology, A 169, 101–8. Regulatory Mechanisms in Insect
Journal of Insect Physiology, 31, 849–56. Schachtner, J. & Braunig, P. (1993). The Feeding, ed. R.F. Chapman & G.de
Oschman, J.J. & Berridge, M.J. (1970). activity patterns of identified neuro- Boer, pp. 190–209. New York:
Structural and functional aspects of secretory cells during feeding behav- Chapman & Hall.
salivary fluid secretion in Calliphora. iour in the locust. Journal of Tjallingii, W.F. & Esch, T.H. (1993). Fine
Tissue & Cell, 2, 281–310. Experimental Biology, 185, 287–303. structure of aphid stylet routes in plant
Parry, D.A. (1983). Labial extension in the Simpson, S.J. (1995). Regulation of a tissues in correlation with EPG signals.
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Comprehensive Insect Physiology, Simpson, S.J. & Ludlow, A.R. (1986). Wilson, E.O. (1971). The Insect Societies.
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Pergamon Press.
3 Alimentary canal, digestion and absorption
[38]
ALIMENTARY CANAL 39
Fig. 3.2. Foregut armature. (a) Sagittal section through the foregut of a locust showing the pattern of cuticular spines on the
intima. Enlargements show details of the spines. In the proventriculus, the spines are replaced by larger sclerotized plates
with backwardly directed teeth at the posterior edges (after Williams, 1954). (b) Longitudinal section of the foregut of
Periplaneta showing the development of the proventriculus to form a grinding apparatus (after Snodgrass, 1935). (c)
Proventriculus of a cockroach slit open and laid flat showing the hexaradial symmetry (after Miller and Fisk, 1971).
larva to eject the contents through the mouth. This appar- lateral diverticulum of the esophagus (Fig. 3.3b,c). The walls
ently has a defensive function. of the crop are folded longitudinally and transversely. The
The crop is a storage organ which in most insects is an folds become flattened as the crop is filled, usually permitting
extensible part of the gut immediately following the esopha- a very large increase in volume. In Periplaneta, however, there
gus (Fig. 3.3a), but, in adult Diptera and Lepidoptera, it is a is little change in volume because when the crop does not
40 ALIMENTARY CANAL, DIGESTION AND ABSORPTION
b)
0.2 m
Fig. 3.5. Midgut epithelium. (a) Diagram of a principal midgut cell. (b) Electron micrograph of the microvilli of a thrips
showing the glycocalyx (g) outside the plasma membrane (p) and the actin filaments (arrows) in the center of a microvillus
(after Del Bene, Dallai & Marchini, 1991).
pads and, from these, folds continue on to the stomodeal in diameter. Each cell has some 9000 microvilli and they
valve. In beetles, the symmetry of the proventricular arma- increase the area of the luminal surface of the cell by over
ture is tetraradial. Strong circular muscles surround the two orders of magnitude. As a result, the total surface area
proventriculus. of the midgut is about 500 cm2 (Fig. 3.6).
The outer surface of the microvilli is covered by the gly-
3.1.2 Midgut cocalyx (Fig. 3.5b) which, in most insects, is a layer of
The cells of the midgut are actively involved in enzyme filamentous glycoproteins, but in some species its compo-
production and secretion, as well as in absorption of nutri- nents form a regular array. In Hemiptera, the glycocalyx is
ents. The majority of the cells, called principal cells, are replaced by lipid membranes that form a tube round each
tall and columnar and the membrane on the luminal side microvillus and, at least in some cases, are separated from the
forms microvilli (Figs. 3.5, 3.6). Each microvillus is sup- plasma membrane by a regular space of 9 or 10 nm. These
ported by a bundle of actin filaments which arise from a membrane tubes extend into the lumen of the midgut when
layer of actin filaments beneath the apical margin of the it contains food (Silva et al., 1995; and see Billingsley, 1990).
cell. When they are synthesizing enzymes, the principal cells
The microvilli greatly increase the area of the cell are characterized by the presence of stacks of rough endo-
membrane through which absorption occurs. In the plasmic reticulum and Golgi bodies. In most insects, syn-
grasshopper, Schistocerca americana, the microvilli of the thesis appears to occur at the time of secretion into the gut
cells in the anterior caeca are about 5 m long and 0.1 m lumen so that stores of enzymes do not accumulate in the cells
42 ALIMENTARY CANAL, DIGESTION AND ABSORPTION
Fig. 3.6. Midgut surface area of a grasshopper. Outline of gut about twice natural size. Sections, all to same scale, through
various parts of the midgut showing the extent of folding of the epithelium. The cells of all parts of the midgut have
microvilli apically and so have very large surface areas. The boxes below show, to scale, the surface area of each part including
the area produced by the microvilli.
(section 3.3.2.5). In a few cases, however, as in Stomoxys, separate from the cell, carrying their contents into the gut
enzymes are stored, probably as inactive precursors (zymo- lumen and ultimately releasing them. This is called apoc-
gens), in membrane-bound vesicles in the distal parts of the rine secretion. It is also possible that vesicles containing
cells. The enzyme is secreted within a few minutes of feeding enzymes move to the microvilli from which they bud off
and, in this species, the cycle of production and release occurs before releasing their contents. Different enzymes may
repeatedly while the meal is digested. In mosquitoes, leave a single cell by different routes, and different methods
however, there is only one synthetic cycle per meal. of secretion may occur in one insect (Wood & Lehane,
Enzyme secretion occurs in several different ways. 1991).
Membrane bound vesicles may move to the periphery of The principal cells of the midgut have a limited life
the cell, fuse with the cell membrane and release their con- and, in most insects, they are continually replaced from
tents into the gut lumen. This process is known as exocyto- regenerative cells at the base of the midgut epithelium
sis (sometimes called eccrine secretion). In addition, (Fig. 3.7a). These often occur in groups, known as nidi,
extensions from the distal parts of the midgut cells may and in some beetles they are found in crypts visible as small
ALIMENTARY CANAL 43
papillae on the outside of the midgut (Fig. 3.7b). In adult apex of the cavity may form a valve which is capable of
Tenebrio all the principal midgut cells are replaced over a opening and closing. These cells create a high concentra-
four-day period. Regenerative cells do not occur in the tion of potassium in the gut lumen (see section 3.4). This is
midgut of cyclorrhaphous Diptera. achieved by two processes occurring at their apical plasma
Endocrine cells are probably present in the midgut epi- membranes: a V-ATPase which pumps H⫹ into the lumen
thelia of all insects. They are probably involved in the and an antiporter at which H⫹ is exchanged for potassium
regulation of enzyme production (see section 21.2.1.5). (Fig. 3.8b). The process consumes large amounts of
Scattered amongst the principal cells of the midgut of energy and it is estimated that it uses 10% of the total ATP
caterpillars are goblet cells in which the luminal plasma produced by the caterpillar.
membrane is invaginated to form a flask-shaped cavity Goblet cells also occur in Ephemeroptera, Plecoptera
(Fig. 3.8). Microvilli extend into the cavity and those at the and Trichoptera, but it is not known if they have a similar
base of the cavity contain mitochondria. Projections at the function to those in the caterpillar.
44 ALIMENTARY CANAL, DIGESTION AND ABSORPTION
Fig. 3.8. Potassium secretion in the midgut of a caterpillar. (a) Diagram of a goblet cell (after Cioffi, 1979). (b) Diagram
showing the movements of ions produced by the V-ATPase and K⫹/H⫹ antiporter at the apical plasma membrane (after
Lepier et al., 1994).
In many insects the midgut has diverticula known as apparently is not present in most Hemiptera. These
ceca, usually at the anterior end (Figs. 3.1, 3.6). There are insects have a membranous covering of the microvilli
two in gryllids and some dipterous larvae; six in Acrididae which may be analogous to a peritrophic envelope. In adult
(grasshoppers), eight in Blattodea and larval Culicidae, Diptera, a peritrophic envelope is absent from unfed
and larger numbers in some Coleoptera and Heteroptera insects, but forms within hours of the insect taking a meal.
where they are variable in position (Fig. 3.9). Only a blood meal induces the formation of the envelope in
The tubular part of the midgut is known as the ventricu- adult mosquitoes; a nectar meal is not followed by its pro-
lus. It exhibits marked anatomical differentiation in the duction in either females or males. In adult Aedes, a com-
Heteroptera (Fig. 3.9), while amongst blood-sucking bugs plete envelope is produced within about 5 hours of
and flies there is regional ultrastructural differentiation of feeding, but in other mosquitoes a longer period is
the principal cells in association with storage, enzyme pro- required.
duction and secretion, and absorption. Sometimes different The envelope is usually made up of a number of separ-
cell types do not form discrete zones in the ventriculus, but ate laminae which are extracellular secretions and should
are scattered through the epithelium as with endocrine cells not be confused with plasma membranes. Sometimes the
and the goblet cells in the midgut of a caterpillar. envelope includes two different types of lamina. Each
Reviews: Billingsley, 1990 – blood-sucking insects; Dow, 1986 – consists of a network of microfibrils, usually chitin, which
structure and function; Harvey & Nelson, 1992 – potassium may be regularly arranged to produce an open lattice
secretion; Lehane & Billingsley, 1996 – structure and function; structure (Fig. 3.10) or randomly oriented. The
Martoja & Ballan-Dufrançais, 1984 – ultrastructure microfibrils are embedded in a matrix of proteins and gly-
coproteins.
3.1.2.1 Peritrophic envelope Peritrophic envelopes are formed in two different ways.
The peritrophic envelope forms a delicate lining layer to In larval Diptera, adult blowflies and Dermaptera, each
the midgut, separating the food from the midgut epi- lamina is secreted by one or more rings of cells at the ante-
thelium (Fig. 3.6). It occurs in most insects, although it rior end of the midgut (Fig. 3.10a). In the larva of Aedes,
ALIMENTARY CANAL 45
for example, the most anterior 8–10 rings of cells in the actively feeding locust, a new lamina is produced about
midgut epithelium, a total of 300–400 cells, produce the every 15 minutes so the peritrophic envelope becomes
entire peritrophic envelope. In this species, the envelope is multilaminar. The inner layers move back with the food as
a single lamina about 0.7 m thick with outer and inner more laminae are produced on the outside, with the result
granular layers bounding a layer with microfibrils that, in the posterior parts of the midgut, the envelope has
arranged in a grid. In contrast, in the earwig, Forficula, more laminae than it does anteriorly. The robustness of the
separate rings of cells in the most anterior part of the envelope varies from species to species. For example,
midgut produce up to four separate laminae in which the amongst the Acrididae (grasshoppers) Locusta, which is
microfibrils form grids. More posterior rings of cells graminivorous, has a thin, delicate envelope, whereas
produce several more very thin laminae in which the Schistocerca, a polyphagous species, has a much thicker and
microfibrils are randomly oriented. The complete per- tough envelope.
itrophic envelope thus consists of several layers of the two It is probable that the permeability properties of per-
types of lamina. These laminae are not, apparently, pro- itrophic envelopes are largely determined by pro-
duced as continuous tubes, but are formed as separate teoglycans. Experimental evidence on various Diptera
patches which join together to form the whole lamina. suggests that molecules with an effective radius of less than
In Orthoptera, Blattodea, larval Hymenoptera and 4.5 nm (with an atomic weight of about 35 kDa) pass
Lepidoptera, and adult Nematocera, the peritrophic through the envelope, but larger molecules do not. In
laminae are produced by the whole midgut epithelium. grasshoppers and larval Lepidoptera, molecules with
Production is not synchronized over the whole midgut diameters of 25–35 nm are the largest that pass through
but, as with laminae produced by anterior rings of cells, the envelopes (Barbehenn & Martin, 1995).
each lamina is formed in patches which join together. At The peritrophic envelope performs a number of
least in some species, the microfibrils forming the laminae different functions. Since it encloses the food bolus within
are assembled at the bases of the microvilli which form a the midgut it effectively separates the gut lumen into ecto-
template for the grid which the microfibrils form (Fig. and endo-peritrophic spaces. These may be important in
3.10c). This process also occurs in the anterior formation the compartmentalization of enzyme activities (section
zone of Forficula. It is known as delamination. In an 3.3.2.4) and also make it possible, in some species, for
46 ALIMENTARY CANAL, DIGESTION AND ABSORPTION
1 m
Fig. 3.10. Peritrophic envelope. (a) Diagram showing the origin of the peritrophic envelope in cells at the anterior end of the
midgut of Forficula (after Peters et al., 1979). (b) Scanning electron micrograph of the peritrophic envelope of Schistocerca.
The envelope has been washed so that only the chitinous lattice remains (after Chapman, 1985a). (c) Diagram showing how
the fibers which will form the lattice of the peritrophic envelope are laid down round the microvilli.
countercurrents to flow within the midgut, increasing the acid, collect in the pockets, apparently being swept in by
efficiency of absorption. In insects eating solid food it pre- the flow of water (see below). The peritrophic envelope of
vents the food particles from coming into contact with the the pockets is pulled out intact as the whole envelope moves
microvilli of the midgut cells, perhaps avoiding damage to down the midgut and the pockets with their contents are
the cells. finally voided with the feces (Bernays, 1981). Tannin mole-
The envelope confers some degree of protection against cules are much smaller than the pores in the envelopes of
potentially harmful chemicals in the food of phytophagous these species, and their failure to pass through must reflect
insects. For example, the envelope of Locusta is permeable the physicochemical properties of the matrix.
to tannic acid which causes lesions in the midgut epi- The relative impermeability of the peritrophic envelope
thelium, eventually leading to the death of the insect. In may also confer some degree of protection against patho-
contrast, the envelope in Schistocerca, which often feeds on genic organisms. The pore sizes are too small to permit the
tannin-containing plants, is impermeable to tannic acid. passage of most bacteria and, in Schistocerca, for example,
Differences in the permeability of the peritrophic envelope the bacterial flora of the midgut, which is obtained adventi-
to tannic acid also occur in caterpillars with different tiously with the food, is entirely contained within the enve-
feeding habits (Barbehenn & Martin, 1992). In lope. Similarly, in older honeybee larvae, Bacillus larvae,
Schistocerca, and other grasshoppers with similar feeding which causes foulbrood in bees, is unable to penetrate the
habits, part of the epithelium of each midgut cecum forms envelope, but young larvae in which the envelope is not yet
a series of small pockets, each lined by the peritrophic enve- developed are highly susceptible to the disease. As in this
lope. Small particles and some chemicals, such as tannic instance, many pathogens of insects are able to circumvent
ALIMENTARY CANAL 47
Fig. 3.12. Rectum. (a) Cross-section of the rectum of a grasshopper showing the six rectal pads. (b) Section through a rectal
pad (after Noirot & Noirot-Timothée, 1976).
Fig. 3.14. Chloride cells in the rectum of a dragonfly larva. (Fig. 17.29 shows the position of the gills within the rectum). (a)
Section of a rectal gill showing the position of the chloride epithelium. Note that tracheal epithelium refers to the epithelium
of the gill through which gas exchange with the tracheae (not shown) occurs. (b) Details of the chloride cells. Notice that the
luminal (water) side of the gill is at the bottom (after Schmitz and Komnick, 1976).
The extrinsic visceral muscles of the hindgut are the full length of the midgut without any insertions into it;
usually present as dilators of the rectum. They are espe- they are inserted anteriorly into the posterior end of the
cially well-developed in larval dragonflies (Odonata) that foregut and posteriorly into the anterior end of the hindgut.
pump water over the gills in the rectum (see Fig. 17.29a). In caterpillars, and probably in other insects, the intrinsic
The intrinsic visceral muscles comprise circular musculature of the hindgut is complex. There are commonly
muscles running round the gut and longitudinal muscles strong muscles associated with the pyloric valve, where the
extending along parts of it. The circular muscles are not Malpighian tubules join the gut. Other specific arrangements
usually inserted into the gut epithelium, but are continu- enable the insect to produce discrete fecal pellets from the
ous all round the gut so that their contraction tends to cylinder of food passing along the gut. Usually the circular
produce longitudinal folding of the epithelium. Round the muscles are outside the longitudinal muscles.
foregut, the circular muscles are external to the longitudi- Ultrastructurally, the extrinsic visceral muscles resem-
nal muscles. They are well-developed around the pharynx ble typical skeletal muscles (section 10.1.2). The intrinsic
and round the proventriculus where this forms a valve or muscles often differ in having 12 actin filaments round
has a grinding function. each myosin filament and the sarcoplasmic reticulum and
Intrinsic muscles are poorly developed round the T-system are reduced compared with skeletal muscles.
midgut. The main longitudinal muscles are outside the cir- Unlike vertebrate visceral muscles, however, insect
cular muscles, although grasshoppers have an inner layer of visceral muscles are striated because their myofilaments
fine muscle fibers in connective tissue adjacent to the midgut are regularly arranged.
epithelium. The longitudinal muscles appear to extend for Review: Smith, 1985 – pumps
50 ALIMENTARY CANAL, DIGESTION AND ABSORPTION
Fig. 3.15. Sucking pumps of fluid-feeding insects. The cibarial muscles are well-developed in all these insects, but the
pharyngeal muscles are also important in larval Dytiscus and mosquito (after Chapman, 1985a).
3.1.5 Innervation of the gut connectives. In Orthoptera and related groups, a median
The muscles of the foregut and anterior midgut are inner- nerve, the recurrent nerve, extends back from the frontal
vated by the stomodeal (or stomatogastric) nervous ganglion beneath the brain to join with the hypocerebral
system. The principal ganglion of this system is the frontal ganglion. This ganglion is closely associated with the
ganglion which lies on the dorsal wall of the pharynx ante- corpora cardiaca, and from it a nerve on each side passes to
rior to the brain (Fig. 3.16). It connects with the trito- the ingluvial ganglion on the side of the crop. From this
cerebrum on either side by nerves called the frontal ganglion, nerves extend back to the midgut. The cell
DIGESTION 51
bodies of most of the motor neurons controlling the hindgut aid the backwards movement of the envelope in
muscles are in the ganglia of the stomodeal system, but a insects which possess them. Blood-sucking bugs, such as
few are in the tritocerebrum. Rhodnius and Cimex, and flies, such as mosquitoes and
The muscles of the hindgut are innervated from the stable flies, which take large, infrequent meals (Table 2.2)
terminal abdominal ganglion. store food in the anterior midgut (Fig. 3.3g). No digestion
There is no evidence of chemosensory neurons associ- occurs here, but water is absorbed. The anterior midgut
ated with the gut, although they do occur in the cibarium also acts as a temporary food store in plant-sucking bugs
(Fig. 2.6). Multipolar cells, which function as stretch (Fig. 3.9).
receptors, are present on the outside of the gut in many The movements of the hindgut are important in the
insects and are involved in monitoring gut fullness. They elimination of undigested material. In Schistocerca the
are most abundant on the foregut, but are also present on ileum usually forms an S-bend and at the point of inflexion
the mid- and hindgut (see Chapman, 1985a). Trichoid the muscles constrict the gut contents. This probably
and campaniform mechanoreceptors are present in the breaks the peritrophic envelope and the food column so
terminal region of the fermentation chamber of scarab that a fecal pellet is formed. Contractions of the posterior
larvae. part of the ileum and the rectum force the pellet out of the
Review: Penzlin, 1985 – stomodeal nervous system anus. In grasshoppers, the feces are enclosed in old per-
itrophic envelope, but in caterpillars the envelope is
broken up in the hindgut.
3.2 PASSAGE OF FOOD THROUGH THE GUT
The time taken for food to pass through the gut is very
Food is pushed back from the pharynx by the muscles of variable. In a grasshopper with continuous access to food,
the pharyngeal pump, and subsequently passed along the liquids from the food reach the midgut and are absorbed
gut by peristaltic movements. These movements are con- within five minutes of the start of a meal, but solid particles
trolled from the stomodeal nervous system. When Locusta may take 15 minutes or more. The food from one meal has
feeds after an interval of several hours without food, the usually left the foregut in about 90 minutes, being pushed
solid food remains in the foregut while the insect is feeding. back by newly eaten food, and by this time some of the
Backward movement of the food bolus begins shortly after meal is present in the hindgut and may appear in the feces
the foregut becomes fully distended. This is at least partly (Fig. 3.17). In the absence of more food, the foregut is
controlled by a hormone from the corpora cardiaca. completely empty in about 5 hours, and the midgut is
In the females of blood-sucking flies that feed on both empty after about 8 hours. In Periplaneta solid food passes
blood and nectar, the destination of the food is determined through the gut in about 20 hours, but some can still be
by its chemical qualities, detected by the receptors on the found in the crop after some days of starvation.
mouthparts. Stimulation with sugars causes the meal to be Termites and larval scarab beetles, which employ
directed to the crop which in flies is a lateral diverticulum micro-organisms to digest cellulose, retain food fragments
of the esophagus. Stimulation with ATP or ADP, but also for long periods in the hindgut.
with dilute sugar solutions, results in the meal going to the
midgut (Schmidt & Friend, 1991). In the blowfly, Phormia,
3.3 DIGESTION
crop emptying is regulated by the osmotic pressure of the
hemolymph. At high hemolymph osmotic pressures, the A large part of the food ingested by insects is macro-
food is passed more slowly to the midgut than at lower molecular, in the form of polysaccharides and proteins,
pressures. Hemolymph osmotic pressure is affected by while lipids are present as glycerides, phospholipids and
that of the food because the sugars are rapidly absorbed. glycolipids. Generally, only small molecules can pass into
Consequently, meals of concentrated sugars are retained the tissues and the larger molecules must be broken down
in the crop for longer periods than meals of dilute sugars. into smaller components before absorption can occur.
The same thing probably occurs in Periplaneta. Enzymes concerned with digestion are present in the
In the midgut, the passage of food is aided by the per- saliva and in the secretions of the midgut. In addition,
itrophic envelope which, as it moves down the gut, carries digestion may be facilitated by micro-organisms in the gut.
the enclosed food with it. Spines on the intima of the Review: Applebaum, 1985
52 ALIMENTARY CANAL, DIGESTION AND ABSORPTION
fecal
pellet test food in
0.5 hours 2.0 hours
fecal pellet
last of
test food
Fig. 3.17. Movement of food through the gut of a grasshopper with continuous access to food (after Baines et al., 1973).
3.3.1 Extra-intestinal digestion restricts their ability to ingest anything except fluids and
Some insects inject saliva into their food before starting to very fine particles, so that food must be pre-digested.
ingest and, because it contains enzymes, considerable There is no evidence that these insects use a venom, in
digestion may occur. Such extra-intestinal (or extra-oral) the sense of a pharmacologically acting chemical, to
digestion may constitute a major part of the total digestion. subdue their prey. Nevertheless, they subdue their prey
This is true in some Hemiptera at all stages of their very rapidly. For example, a cockroach captured by the
development, in adult Asilidae and Empididae amongst the reduviid, Platymeris, stops its convulsive struggling in
Diptera, and in the larvae of Neuroptera and some beetles 3–5 s, and is completely motionless after 15 s. This is
such as Dytiscus and the Lampyridae. Extra-intestinal apparently achieved through the rapid action of the
digestion is probably also significant in some adult carabid enzymes which the bugs inject into the prey. Periods
beetles, although the bulk of digestion occurs in the gut. when enzymes are injected into the prey are separated
Amongst the plant-sucking Hemiptera, extra- by periods in which the enzymes and liquified contents
intestinal digestion is most significant amongst seed- of the prey are ingested. The reduviid, Zelus, is thus able
feeding species such as Oncopeltus and Dysdercus, to remove a very large proportion of the protein and
although it may also be important in species feeding glycogen content of a caterpillar in the first 45 minutes
from the parenchyma of plants. However, it is amongst of feeding, but lipid is removed more slowly (Fig. 3.18).
the predaceous Heteroptera that extra-intestinal diges- Predaceous larval beetles and Neuroptera have biting
tion is most widespread. Predators occur in 30 families mandibles with which they capture their prey (Fig. 2.5),
of Heteroptera. Belostomatidae, Reduviidae and and through which enzymes are injected into the prey and
Nabidae are families in which all the species are pre- the digested contents withdrawn. Beetles have no salivary
daceous or feed on vertebrate blood; Lygaeidae and glands so it must be presumed that, in this case, the
Pentatomidae are families in which some species are enzymes originate in the midgut. Adult carabids in the
predaceous. The stylet structure of most of these insects tribes Carabini and Cychrini masticate their prey before
DIGESTION 53
Fig. 3.19. Enzyme activity. The relative activities of amylase and trypsin in insects with different feeding habits. The grain
beetles are species of Sitophilus (based on Baker, 1986).
Table 3.1. Enzymes digesting proteins and carbohydrates in insects with different feeding habits. Numbers show numbers of different enzymes that are known to be present
Food Insects Order Trypsin Chymotrypsin Cathepsin Metalloproteinase Amino- Carboxy- Amylase ␣  ␣ 
Notes:
⫹⫽One or more enzymes present.
0⫽Enzyme looked for, but not found.
–⫽No data.
*⫽Present, but may be from symbiont.
L, Larva; A, adult.
DIGESTION 55
the molecule. Within these general categories, the enzymes addition to those normally present in caterpillars, it
are classified according to the nature of their active sites and possesses a highly active cysteine desulfhydrase which pro-
the sites at which they cleave protein molecules. duces hydrogen sulfide from cysteine. This contributes to
The principal endopeptidases in the majority of the strong reducing conditions in the gut (see below) which
insects are the serine proteases, trypsin and chy- promote the breaking of disulfide bonds in the keratin
motrypsin, which have serine at the active site. Trypsin (Yoshimura et al., 1988). Similar conditions are found in
cleaves peptide linkages involving the carboxyl groups of other insects that feed on wool or feathers (see Table 3.2).
arginine and lysine residues. Chymotrypsin is less
specific, cleaving bonds involving the carboxyl groups of 3.3.2.2 Digestion of carbohydrates
tyrosine, phenylalanine and tryptophan preferentially, Carbohydrates are generally absorbed as monosaccharides
and bonds involving other amino acid residues more so disaccharides and polysaccharides in food require diges-
slowly. Usually both types of enzyme are present in any tion. The polysaccharide cellulose is a major constituent of
insect with serine proteases (Table 3.1). However, in green plants, but although many insects are phytophagous,
many Coleoptera and in blood-sucking Hemiptera, the relatively few of them are able to utilize cellulose. Those
main endopeptidases have cysteine or aspartic acid at that do, nearly always depend on micro-organisms to digest
their active centers (Murdock et al., 1987). They are it (see below). However, starch and glycogen, the main
called cathepsins. storage polysaccharides of plants and insects, respectively,
Exopeptidases fall in two categories: carboxypeptidases are digested by amylases that hydrolyse 1–4-␣-glucosidic
that attack peptides from the -COOH end, and amino- linkages. There may be separate endo- and exo-amylases,
peptidases that attack the chain from the -NH2 end. acting on starch internally or terminally.
The common disaccharides sucrose and maltose
R R
contain a glucose residue linked to another sugar by an ␣-
CH CH linkage:
NH2 CO NH CO
α-link
CH2OH
aminopeptidase
attacks here O HOCH2 O
R R
OH O HO
HO CH2OH
CH CH
OH OH
NH CO NH CO β-link α-link
glucose fructose
CH2OH CH2OH
SUCROSE
endopeptidase O O
attacks here
R R OH OH
O
HO OH
CH CH OH OH
glucose glucose
NH CO NH COOH
MALTOSE
carboxypeptidase
attacks here
These are digested by ␣-glucosidases (enzymes attacking
the ␣-linkage). As with the proteolytic enzymes, ␣-glu-
Keratin Keratin is a protein occurring in wool, hair and cosidases may exhibit different substrate specificities. For
feathers. Hard keratins contain 8–16% cystine, and example, a trehalase is often present, although it is not
disulfide linkages between cystine residues render the clear why this should occur in insects that feed on plants
protein very stable. Nevertheless, a number of insects nor- where trehalose is not found.
mally feed on keratinous materials. These include larvae of The naturally occurring -glucosides (e.g., salicin and
the clothes moth (Tineola), carpet beetles (Dermestidae) arbutin) are usually of plant origin and the highest -glucosi-
and numerous biting lice (Ischnocera). Tineola larva has a dase activity is found in phytophagous insects. Cellobiose is a
complex mixture of proteolytic enzymes (Table 3.1). In product of cellulose digestion and a cellobiase is often present
56 ALIMENTARY CANAL, DIGESTION AND ABSORPTION
even in insects where cellulose digestion is not known to Cellulose Cellulose is polymer of glucose in which the
occur. ␣- and -galactosidases are also often present. glucose molecules are joined by –1–4 linkages. The
In the hydrolysis of carbohydrates, water is the typical chains of cellulose are unbranched and may be several
acceptor for the sugar residues: thousand units long:
CH2OH
CH2OH OH CH2OH
O HOCH2 O
O O
+ H2O O OH O
OH O HO
HO CH2OH OH O OH
HO O
OH OH
OH CH2OH OH
sucrose
CH2OH
CELLULOSE
O HOCH2 O
+
OH HO β-link
HO OH CH2OH
CH2OH OH
OH OH
O
glucose fructose O OH
OH
HO OH
but other sugars may equally well act as acceptors with the O
OH CH2OH
formation of oligosaccharides. Thus, in the hydrolysis of glucose glucose
sucrose, other sucrose molecules may act as acceptors to CELLOBIOSE
form the trisaccharides glucosucrose and melezitose. This
process is known as transglucosylation and a similar Hydrogen bonds occur within and between cellulose mole-
process occurs in the hydrolysis of maltose. In some cules, resulting in a crystalline state which contributes to
aphids glucosucrose and melezitose appear to be pro- the resistance of cellulose to digestion. Three classes of
duced by two ␣-glucosidases with different acceptor enzyme are involved in its hydrolysis: endoglucanases,
specificities for the sucrose molecule. It is probably for this which attack the bonds between glucose residues within
reason the melezitose is a common component of aphid the chain; exoglucanases that attack bonds near the ends of
honeydew. the cellulose molecule; and -glucosidases that hydrolyze
cellobiose. Exoglucanases are usually more active against
crystalline cellulose than endoglucanases.
Amongst the termites, species in all the families except
Termitidae have huge numbers of flagellate protozoans in
the paunch (Fig. 3.3f). These organisms may constitute
more than 25% of the wet weight of the insect. Many
different species of flagellate may be present in one species
of termite, but the species are, in general, only found in
termites. The protozoans engulf fragments of plant
material and ferment the cellulose, producing acetate and
other organic acids, carbon dioxide and hydrogen.
Fermentation is an anaerobic process and conditions in the
paunch are highly reducing (see below). The organic acids
are absorbed in the hindgut and provide a large proportion
of the respiratory substrate used by the insect. These
insects probably do produce cellulose-digesting enzymes
themselves, but their activity is insufficient for the termites
to sustain themselves without the aid of the symbionts.
Flagellates also occur in the hindgut of the wood-eating
cockroach, Cryptocercus.
DIGESTION 57
enzyme activity (% of max) 100 Enzymes are most active only within a limited range of
pH (Fig. 3.23). Most insects have enzymes with optima at
75 pH 6–7, but in caterpillars optimal activity occurs at about
pH10. These optima correspond with the conditions
50 found in the guts of various insects.
pH often varies along the length of the gut. In the foregut
25 it is greatly influenced by the food and varies with diet. For
example, the foregut pH of a cockroach that has eaten a diet
0 rich in protein is about 6.3; after feeding on maltose the pH is
0 10 20 30 40 50 60
5.8 and, after glucose, 4.5–4.8. Although the midgut pH may
temperature ( o C)
also vary with the diet, it is usually buffered to maintain a rel-
Fig. 3.22. Enzyme activity in relation to temperature. The activity atively stable level. In most insects it is in the range pH 6.0 to
of the ␣-glucosidase of a locust (after Evans and Payne, 1964). 8.0, but larval Lepidoptera are marked exceptions. Here the
pH is always above 8.0 and may be as high as 12.0. This is
The midgut environment Enzymes function efficiently well above the pH of the food, which is usually less than 6.0.
only within limited ranges of temperature, pH and redox Mosquitoes have little buffering facility, and after a blood
potential. meal midgut pH rises to 7.3, the normal value for blood.
Enzyme activity increases with temperature, but at Variation may occur along the length of the midgut. In cater-
higher temperatures the enzymes are denatured. pillars, it is lower at either end than in the middle, whereas in
Consequently, activity rises to a maximum and then larval Lucilia the converse is true. The hindgut is usually
declines as the rate of denaturing becomes faster (Fig. slightly more acid than the midgut, partly due to the secre-
3.22). Maximum activity of most insect digestive enzymes tions of the Malpighian tubules.
is in the range 35–45 °C. Below 10 °C activity is usually As well as affecting the activity of the insect’s own
slight, and above 50 °C enzymes are denatured so rapidly enzymes, the pH of the midgut influences the potentially
that very little digestion will occur. These changes are harmful effects of some ingested compounds (Felton,
reflected in the thermal limits for survival and in thermo- Workman & Duffey, 1992).
regulatory behavior (Chapter 19). Redox potential is a measure of the oxidizing or
75 75
50 50
25 25
0 0
2 4 6 8 10 12 2 4 6 8 10 12
pH pH
Fig. 3.23. Enzyme activity in relation to pH. (a) Proteolytic activity of Rhodnius, a blood-sucking bug; Glossina, a blood-
sucking fly; larva of Trichoplusia, a leaf-eating caterpillar. The endopeptidases of Rhodnius are cathepsins, those of Glossina
and Trichoplusia are trypsins. (b) Amylase activity of the larva of Rhynchosciara, a fly larva feeding on decaying plant material;
larva of Bombyx, a leaf-eating caterpillar.
60 ALIMENTARY CANAL, DIGESTION AND ABSORPTION
Table 3.2. Redox potentials in different parts of the alimentary canals of different insects
Redox potential
Paunch/fermentation
Food Species Order Foregut Midgut chamber Hindgut
Notes:
⫹⫹⫹ Strongly oxidizing.
⫺⫺⫺ Strongly reducing.
0 Variably oxidizing/reducing.
⫻ Not present.
· No data.
3.4 ABSORPTION
reducing conditions in a system. A high positive potential
indicates strongly oxidizing conditions, a high negative The products of digestion are absorbed in the midgut, but
potential indicates strongly reducing conditions. It is some absorption, especially of salts and water, also occurs
probable that in most insects oxidizing conditions nor- in the hindgut. The cells in the midgut concerned with
mally prevail throughout the gut (Table 3.2), but in insects absorption are often the same cells that produce enzymes
feeding on substances that are intractable to digestion, in a different phase of their cycle of activity.
such as wood, wool, or keratin, strongly reducing condi- Absorption may be a passive or an active process. Passive
tions are produced in a part of the gut. In some of these absorption depends primarily on the relative concentra-
cases, as in Zootermopsis and the larva of Oryctes, micro- tions of a compound inside and outside the gut, diffusion
organisms which are effective only under anaerobic condi- taking place from the higher to the lower concentration. In
tions are believed to maintain the reducing conditions. In addition, in the case of electrolytes, the tendency to main-
other cases, it is believed that the insect itself maintains the tain electrical equilibrium inside and outside the gut epi-
conditions. It is not known why the caterpillar of Manduca thelium will interact with the tendency to diffuse down the
should maintain high reducing conditions in its midgut, concentration gradient. These two factors together consti-
while other caterpillars, such as Danaus, do not. It is likely tute an electrochemical potential (Fig. 3.24).
that the extent of oxidizing or reducing conditions will Active absorption depends on some metabolic process to
affect the potential toxic activity of plant secondary com- move a substance against its concentration gradient. In the
pounds in the food of phytophagous insects (Appel and midgut of caterpillars, and probably of other insects, the
Martin, 1990). energy for these processes is derived from a V(vacuolar)-
Reviews: Chapman, 1985b – regulation of enzyme production; type ATPase in the apical plasma membranes. This pumps
Dow, 1992 – caterpillar midgut pH protons from the cells into the gut lumen and the protons
ABSORPTION 61
K+
posterior midgut
ileum
rectum
basal
c) lamina
filter
chamber
posterior
midgut Malpighian
tubule
anterior
midgut ileum
water
movement
with a large accessory salivary gland. After feeding, a clear pressure. Chloride moves passively into the lateral inter-
fluid is exuded from the mouthparts suggesting that water is cellular spaces and sodium is pumped out by sodium/potas-
withdrawn from the midgut directly to the salivary glands sium ATPase so that water is drawn osmotically into the
and then eliminated via the mouthparts. spaces. Hydrostatic pressure forces the solution out to the
Water absorption from blood stored in the anterior hemolymph, but ions are resorbed as the fluid passes out
midgut of Rhodnius is dependent on the active movement from between the principal cells. This permits the recycling
of sodium into the hemocoel. It is believed that, in this of the ions and the maintenance of absorption.
case, the sodium is transported out of the cell by Reviews: Chapman, 1985a – structure; Phillips & Audsley, 1995
sodium/potassium exchange pumps in the basal plasma – physiology; Phillips et al., 1986, 1988 – physiology
membrane (Farmer, Maddrell & Spring, 1981).
3.4.2 Absorption of organic compounds
3.4.1.2 Water absorption from the hindgut The forward flow of water outside the peritrophic envelope
In terrestrial and saltwater insects water is absorbed from produced by its absorption in the anterior parts of the
the rectum. Here, as in the midgut, V-ATPase in the apical midgut carries with it the products of digestion, and, where
plasma membrane probably provides the energy that drives they occur, the midgut ceca are a primary area of absorption.
the inward movement of ions and amino acids, principally In well-fed grasshoppers, the water is derived directly from
chloride and proline in the locust (Fig. 3.26). Water moves the food, but in insects deprived of food, and in cock-
across the epithelium due to the increased osmotic roaches, water is drawn forwards as it leaves the Malpighian
ABSORPTION 63
gut lumen
ion
b) channel
+ + +
amino + + -
H NH4 Na acids Na K Cl
V - ATPase
electrogenic
pump
cAMP
+ +
Na , K - ATPase
+
K
- - + + -
HCO3 Cl amino Na K Cl
acids
chloride transport
stimulating hormone
hemocoel
64 ALIMENTARY CANAL, DIGESTION AND ABSORPTION
tubules. In larval Diptera, and perhaps in some other concentration of glucose in the blood never builds up.
insects, the forward movement occurs in the ectoperitrophic Mannose and fructose are absorbed in a similar manner, but
space, while fluid in the endoperitrophic space moves back- more slowly than glucose because their conversion to tre-
wards. This counter current probably improves the halose is less rapid. As a result, their concentration gradi-
efficiency of utilization of the digested materials in the gut. ents across the gut wall are less marked. Absorption of water
from the lumen of the gut also tends to maintain a relatively
Amino acids The absorption of amino acids is best under- high concentration of sugars in the gut.
stood in caterpillars. If amino acids are present in high Glycogen appears in the posterior midgut cells soon
concentration in the gut lumen they diffuse across the epi- after glucose is ingested by larval Aedes. It is possible that
thelium down a concentration gradient; at low concentra- rapid conversion to glycogen might maintain a concentra-
tions, amino acid absorption occurs at symports coupled tion gradient of glucose inward from the gut lumen. In
with the movement of a cation, usually potassium, into the Phormia and other dipterous larvae, however, the
cell. Several types of symport are present, differing in their concentration of glucose in the hemolymph is normally
specificity for amino acids, and cells in different parts of high, so glucose absorption must entail another, possibly
the midgut vary in their ability to take up different amino active, process.
acids (Wolfersberger, 1996).
Different amino acids enter the hemocoel at different Lipids Lipids appear to be absorbed primarily as fatty
rates and in different amounts relative to those present in acids. In Stomoxys, fatty acids are absorbed in the posterior
the gut lumen, partly as a result of their differential uptake, zone of the midgut and then incorporated into phospho-
but also because they may be metabolized within the gut lipids and triacylglycerides. In caterpillars, the turnover of
epithelium. In the locust, glutamate is changed to alanine triacylglycerides is rapid and it appears that they are trans-
and glutamine, and it is these that reach the hemocoel; ported to the basal parts of the cell where they are actively
little or no glutamate does so. This is important because exported as diacylglycerides. The turnover of phospho-
glutamate is a neural transmitter at nerve/muscle junc- lipids is slower and substantial amounts remain in the
tions and this function is impaired if glutamate is present midgut cells 24 hours after a meal (Turunen &
in the hemolymph. Chippendale, 1989). At times, the rate of export of lipids is
Amino acids form part of the primary urine produced unable to keep pace with the rate of production of inter-
in the Malpighian tubules (section 18.3.1). Consequently, mediates and these are temporarily stored in lipid spheres.
significant quantities reach the hind gut and are resorbed Sterols appear to be absorbed unchanged, but, in some
in the rectum. In the locust, glycine, serine, alanine and caterpillars, sterols are esterified in the gut cells.
threonine are actively resorbed into the cells of the rectal
pads by a sodium-cotransport system in the apical mem- 3.4.3 Absorption of inorganic ions
brane, but uptake of proline is independent of sodium and For sodium to move from the gut lumen into the hemolymph
is probably cotransported with protons (Phillips & of a locust, it must move against the electrochemical gradient
Audsley, 1995). From these cells, amino acids probably (Fig. 3.24). Energy for this active movement is provided by
enter the hemocoel passively, moving down a concentra- V-ATPase pumps in the apical plasma membranes of the
tion gradient. Some metabolism of amino acids occurs in anterior ceca, and by major sodium/potassium exchange
the rectal cells. Proline is the major metabolic substrate in pumps in the basal plasma membranes of the rectal cells.
the locust rectum, and, as in the midgut, glutamate is com- Potassium, on the other hand, probably moves passively
pletely metabolized. down its electrochemical gradient into the hemocoel. The
electrochemical gradients for chloride and calcium ions are
Carbohydrates Carbohydrates are absorbed mainly as less extreme (Dow, 1981). In the rectum, chloride ions are
monosaccharides. In some cases, at least, it is a passive actively removed from the lumen by pumps in the apical
process depending on diffusion from a high concentration membranes of the cells and pass passively from the cells to
in the gut to a low one in the hemolymph. This is facilitated the hemolymph. Calcium is actively moved from the gut
by the immediate conversion of glucose to the disaccharide lumen to the hemocoel by cells in the midgut.
trehalose in the fat body surrounding the gut so that the Review: Taylor, 1986 – calcium
EFFICIENCY OF DIGESTION AND ABSORPTION 65
Table 3.3. Average values for efficiency with which foods are digested and absorbed
(expressed as approximate digestibility, AD) by larval insects
Other insects
parasitoids 215 Hymenoptera 68
predators 212 Various 85
Detritus 220 Coleoptera 32
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4 Nutrition
Nutrition concerns the chemicals required by an organism digest it. Proteins vary considerably in the extent to
for its growth, tissue maintenance, reproduction and the which an insect is able to digest them. This may depend
energy necessary to maintain these functions. Many of on the frequency with which appropriate points of attack
these chemicals are ingested with the food, but others are occur on the protein and the extent to which these are
synthesized by the insect itself. In some insects, micro- protected by the protein’s structural configuration
organisms contribute to the insect’s nutrient pool. (Broadway & Duffey, 1988). Although proteins contain
some 20 different amino acids, usually only 10 of these are
essential in the diet; the others can be synthesized or
4.1 NUTRITIONAL REQUIREMENTS
derived from these 10. The essential amino acids for
Most insects have qualitatively similar nutritional require- insects are the same as those needed by rats. They are
ments since the basic chemical composition of their tissues listed in Table 4.1 and Fig. 4.1. In general, the absence of
and their metabolic processes are generally similar. Most any one of these amino acids prevents growth. Some
of these requirements are normally met by the diet. Some insects have essential requirements for additional amino
chemicals can only be obtained in the diet: they are essen- acids. Proline is the most common of these. For example,
tial (Table 4.1). Others may be synthesized by the insect it is essential for the development of the mosquito
from dietary components. The dietary requirements of a (Culex), and for several other Diptera as well as the silk-
species may sometimes be obscured due to chemicals worm (Bombyx). In some other insects it is necessary for
having been accumulated and passed on from a previous good growth and survival, although it is not absolutely
generation. essential. Aspartic acid or glutamic acid are also essential
Despite the overall similarities, major differences in for Phormia and the silkworm.
nutritional requirements do occur. These may be the result Although other amino acids are not essential, they are
of evolutionary changes associated with feeding on sub- necessary for optimal growth because their synthesis or
strates with quantitatively, and sometimes qualitatively, conversion from essential amino acids is energy consum-
different balances of nutrient chemicals. ing and necessitates the disposal of surplus fragments.
Reviews: Dadd, 1977, 1985; Reinecke, 1985 Consequently, alanine and glycine or serine are necessary,
in addition to the essential amino acids, for optimal
4.1.1 Amino acids growth of the silkworm. These non-essential amino acids
Amino acids are required for the production of proteins may comprise over 50% of the total amino acids neces-
which are used for structural purposes, as enzymes, for sary to produce optimal growth on an artificial diet (Fig.
transport and storage, and as receptor molecules. In addi- 4.1).
tion, some amino acids are involved in morphogenesis. The extent to which the synthesis of non-essential
Tyrosine is essential for cuticular sclerotization (section amino acids can occur may be limited by the abilities of
16.5.3) and tryptophan for the synthesis of visual screen- insects to make certain chemical structures. Tyrosine is a
ing pigments (Fig. 25.6). Others, ␥-aminobutyric acid and key amino acid in the process of cuticular sclerotization,
glutamate, are neurotransmitters (section 20.2.3.1), and, but insects cannot synthesize its aromatic ring.
in some tissues and some insects, proline is an important Consequently, tyrosine can only be synthesized from com-
energy source. pounds with the same basic structure. Phenylalanine is
Amino acids are usually present in the diet as proteins another aromatic amino acid from which tyrosine is often
and the value of any ingested protein to an insect depends derived, but some polyphagous grasshoppers are able to
on its amino acid content and the ability of the insect to use some phenolic compounds, such as protocatechuic
[69]
Table 4.1. Qualitative dietary requirements of the larvae of insects with different feeding habits (data from Dadd, 1977)
Amino acids
arginine* ⫹ ⫹ ⫹ ⫹ ⫺ ⫹ ⫹ ⫹
histidine* ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹
isoleucine* ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹
leucine* ⫹ ⫹ ⫹ ⫹ ⫺ ⫹ ⫹ ⫹
lysine* ⫹ ⫹ ⫹ ⫹ ⫾ ⫹ ⫹ ⫹
methionine* ⫺ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹
phenylalanine* ⫺ ⫹ ⫹ ⫹ ⫺ ⫹ ⫹ ⫹
threonine* ⫹ ⫹ ⫹ ⫹ ⫺ ⫹ ⫹ ⫹
tryptophan* ⫹ ⫹ ⫹ ⫹ ⫺ ⫹ ⫹ ⫹
valine* ⫹ ⫹ ⫹ ⫹ ⫺ ⫹ ⫹ ⫹
alanine ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺
aspartic acid ⫺ ⫾ ⫺ ⫹ ⫺ ⫺ ⫺ ⫺
cystine ? ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹
glutamic acid ⫺ ⫾ ⫺ ⫾ ⫺ ⫺ ⫺ ⫺
glycine ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫾ ⫾
proline ? ? ⫺ ⫹ ⫺ ⫺ ⫺ ⫹
serine ? ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺
tyrosine ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺ ⫺
Carbohydrates ⫹ ⫺ ⫹ · ⫹ · ⫾ ·
Fatty acids
linoleic or linolenic ⫹ ⫺ ⫹ ⫹ ⫺ · ⫺ ⫺
others · · · · · · ⫾ ·
Sterols ⫹ ⫹ ⫹ ⫹ ? · ⫹ ⫹
Lipogenic compounds
myo-inositol ⫹ ⫹ ⫹ · ⫹ · ⫺ ·
choline ⫹ ⫹ ⫹ · ⫹ · ⫹ ·
Nucleic acids . ? · · ⫺ · ⫾ ⫹
Inorganic compounds
sodium · · ⫹ ⫹ · · · ·
potassium ⫹ · ⫹ ⫹ ⫹ · ⫹ ·
calcium ⫹ · · ⫹ ⫹ · · ·
chloride ⫹ · · ⫹ · · · ·
iron · · ⫹ ⫹ ⫹ · · ·
zinc ⫹ · ⫹ ⫹ ⫹ · ⫹ ·
manganese ⫹ · ⫹ ⫹ ⫹ · ⫹ ·
Notes:
⫹ Essential. ⫾ Not essential, but improves growth. * Rat essentials.
- Not needed. ? Uncertain.
· Not known. a Micro-organism present in these insects.
72 NUTRITION
arginine
histidine
essential amino acids
isoleucine
leucine
lysine
methionine
phenylalanine
threonine
tryptophan
valine
alanine
non-essential amino acids
aspartic acid
*
cysteine/cystine
glutamic acid
*
proline
*
glycine
serine
tyrosine
0 5 10 15 0 5 10 15 0 5 10 15 20 25 30 35
% of total amino acids
essential for this species
*
Fig. 4.1. Quantitative requirements for amino acids required in artificial diets to produce optimal growth of different insects.
Expressed as a percentage of all amino acids in the diet (data from Dadd, 1985).
acid and gallic acid, in cuticle sclerotization (section Sulfur-containing amino acids are only produced from
16.5.3) so conserving phenylalanine and tyrosine for other amino acids containing sulfur. Consequently, cystine
protein synthesis. These compounds are non-nutrient and and cysteine can be synthesized from methionine and are
potentially harmful for many other insects. not necessary in the diet if there is ample methionine.
NH2 NH2
HO CH 2 C COOH CH 3 S CH 2 CH 2 C COOH
H H
tyrosine methionine
NH2 NH2
CH 2 C COOH HS CH 2 CH 2 C COOH
H H
cystine
phenylalanine
NH2 H
HO HO
HOOC C CH 2 S S CH 2 C COOH
HO COOH HO COOH
H NH2
HO cysteine
protocatechuic acid gallic acid
NUTRITIONAL REQUIREMENTS 73
aspartic α - ketoglutaric
acid acid
CH (NH2 ).COOH
CO.COOH Fig. 4.2. Quantitative effect of sucrose in artificial diets on the
+ CH2
growth from hatching of Schistocerca (after Dadd, 1960).
CH2 .COOH
CH2 .COOH
oxaloacetic glutamic sion probably occurs in most insects, and some species grow
acid acid
readily on artificial diets containing no carbohydrates. This is
Glutamate often plays a central role in these reactions and true of the larva of the screw-worm fly, which feeds on live
serves both to incorporate nitrogen into the system and to animal tissues, and carbohydrate can be entirely replaced by
distribute it among different amino acids. wax in the diet of the wax moth, Galleria.
Nevertheless, most insects so far examined require
alanine, transamination leucine and other some carbohydrate in the diet, and grow better as the pro-
aspartate amino acids
portion is increased. Schistocerca for example, needs at
tra
io
io
ns
at
at
am
in
amino acid
in
in
oxidases
at
ns
ns
io
tra
NH3.ATP
glutamine glutamate keto acids growth is optimal with 70% carbohydrate.
The utilization of different carbohydrates depends on
NAD
glutamate the insect’s ability to hydrolyse polysaccharides (section
dehydrogenase
NADH 2 3.3.2.2), the readiness with which different compounds
ketoglutarate are absorbed, and the possession of enzyme systems
Transamination is a common phenomenon and, in the capable of introducing these substances into the metabolic
silkworm, 19 different amino acids are known to act as processes. Some insects can use a very wide range of car-
donors of amino groups in transamination reactions bohydrates, probably because they are capable of digest-
ing the more complex structures. Tribolium, for example,
4.1.2 Carbohydrates can utilize starch, the alcohol mannitol, the trisaccharide
Insect cuticle characteristically contains chitin, a poly- raffinose, the disaccharides sucrose, maltose and cel-
saccharide (section 16.2.1.1). Carbohydrates are also used as lobiose, as well as various monosaccharides. Other insects
fuels by a majority of insects. They may be converted to fats, feeding on stored products, and some phytophagous
and may contribute to the production of amino acids. They insects, like Schistocerca and Locusta, can also use a wide
are, therefore, important components of the diets of most range of carbohydrates, but other phytophagous insects
insects, but they are not necessarily essential because they can are more restricted. The grasshopper, Melanoplus, is
be synthesized from fats or amino acids. Some such conver- unable to utilize polysaccharides, and stem-boring larvae
74 NUTRITION
of the moth, Chilo, can only use sucrose, maltose, fructose known as eicosanoids, stimulate oviposition in crickets and
and glucose. Most insects are unable to utilize cellulose may be important in the reproduction of all insects. They
and other plant polymers because they lack the enzymes to may also be important in thermoregulation and in lipid
digest them. In some species, however, these substances mobilization and there is some evidence that eicosanoids
are made available to the insect by the activities of micro- mediate the immune response of caterpillars to bacteria in the
organisms. Pentose sugars do not require digestion since hemolymph (Stanley-Samuelson et al., 1991).
they are monosaccharides, but nevertheless do not gener- Some insects, like the cockroach, Periplaneta, and the
ally support growth and may be actively toxic, perhaps cricket, Acheta, are able to synthesize polyunsaturated fatty
because they interfere with the absorption or oxidation of acids from dietary acetate, and this may also be true of some
other sugars. flies. Synthesis generally involves the elongation of existing
There may be differences in the ability of larvae and components by the condensation of 2-carbon units. This
adults to utilize carbohydrates. For instance, the larva may be followed by desaturation to produce compounds
of Aedes can use starch and glycogen, but the adult cannot. with double bonds; thus stearic is converted to oleic acid.
Many other species, however, do have a dietary require-
4.1.3 Lipids ment for small quantities of certain polyunsaturated fatty
acids. Lepidoptera, in general, appear to require linolenic
Fatty acids, phospholipids and sterols are components of or linoleic acid in the diet. A shortage of linoleic acid in the
cell walls as well as having other specific functions. Insects diet of Ephestia results in the moths emerging without
are able to synthesize many fatty acids and phospholipids scales on the wings because the scales do not separate from
so they are not usually essential dietary constituents, but the pupal cuticle. Some insects are able to synthesize C20
many insects do require a dietary source of poly- acids from C18 acids (linoleic or linolenic acids), but others
unsaturated fatty acids, and all insects require sterols. require a dietary source (Stanley-Samuelson et al., 1992).
Larval mosquitoes, for example, require a dietary source of
Fatty Acids Fatty acids form an homologous series with the C20 fatty acids. Without them, the emerging adults are
general formula CnH2n⫹1COOH. In the insects, they are weak and unable to fly. The number and position of the
present mainly as diacylglycerides and triacylglycerides: double bonds in the ingested fatty acids is critically impor-
tant (Dadd, Kleinjan & Stanley-Samuelson, 1987).
CH2O - CO - R CH2O - CO - R
Mosquito larvae require a double bond in the 6 position,
CH2O - CO - R' CH O - CO - R' while larval Galleria mainly utilize fatty acids with a double
bond in the 3 position (Fig. 4.3).
CH2O - CO - R"
carboxyl methyl
end ω6 ω3 end activity in
Galleria Culex
α - linolenic acid ++ +
++ +
++ +
docosahexaenoic acid - ++
eicosapentaenoic acid - ++
arachidonic acid - ++
homo - γ - linolenic acid - ++
γ - linolenic acid - ++
+ +
linoleic acid + +
oleic acid - -
double bond ++ active
+ some activity
- not active
Fig. 4.3. Fatty acid utilization (shown as activity) by larvae of Culex and Galleria. The boxed sections emphasize
arrangements of double bonds that are important to the two insects. Culex larvae utilize acids with double bonds in different
positions from those utilized by Galleria larvae (after Dadd, 1985).
A few insects with specialized feeding habits use other insects. Without it, they do not develop their normal yellow
sterols preferentially, reflecting the absence of cholesterol or green colors and melanization is also reduced.
from their normal food. Drosophila pachea feeds on a Vitamin E (␣-tocopherol) is necessary for reproduction
cactus, Lophocerus schottii, in which the only sterols are in at least some insects. It improves the fecundity of some
lophenol and schottenol which it utilizes, but it is unable to moths and beetles, and, in its absence, spermatogenesis in
use any of the usual plant sterols, including cholesterol. the house cricket is halted after spermatid formation
Another species, the ambrosia beetle, Xyleborus, that feeds (McFarlane, 1992).
on a symbiotic fungus (see below), can utilize cholesterol, Reviews: Bernays, 1992 – sterol requirements of phytophagous
but this compound alone is not sufficient for the beetle to insects; Stanley-Samuelson, 1993, 1994 – eicosanoids; Svoboda &
complete its development; ergosterol or 7-dehydrocholes- Thompson, 1985 – sterol metabolism
terol, typical fungal sterols, are essential.
4.1.4 Water-soluble growth factors
Fat-soluble vitamins -carotene (provitamin A) is proba- B vitamins The B vitamins are organic substances, not
bly essential in the diet of all insects because it is the func- necessarily related to each other, which are required in
tional component of visual pigments (section 22.2.3). It small amounts in the diet because they cannot be syn-
probably also has other functions. For example, the eggs of thesized. They often function as cofactors of the enzymes
Schistocerca normally contain enough -carotene to permit catalyzing metabolic transformations. All insects require a
growth of the larvae, but in insects reared on a carotene- source of seven such compounds, either in the diet or
free diet from eggs already deficient in carotene, growth is produced by associated micro-organisms. These seven are:
retarded and the molt delayed. In addition, the insects are thiamine, riboflavin, nicotinic acid, pyridoxine, pan-
smaller and less active than usual. -carotene is also com- tothenic acid, folic acid and biotin.
monly involved in the normal pigmentation of leaf-eating Some of these compounds are known, in addition, to
Table 4.2. Sterol utilization by insects with different feeding habitsa
Cholesterol ⫹ ⫹ ⫹ ⫹ ⫹ · ⫹ ⫺ ⫹ ⫹
7–Dehydrocholesterol ⫺ · ⫺ · · · ⫺ · · ⫹
Ergosterol ⫺ ⫾ ⫺ · · ⫺ ⫹ ⫺ ⫺ ⫺
-Sitosterol ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫺ ⫺ ⫺
Stigmasterol ⫹ · ⫺ ⫹ ⫹ ⫹ ⫹ ⫺ · ⫺
Campesterol · · · ⫹ ⫹ ⫹ · · · ·
Spinasterol · · ⫺ ⫹ ⫹ ⫺ · · · ·
Notes:
a Some of the structures are shown in Fig. 4.4.
b See text.
⫹ Utilizable.
⫾ Probably utilizable.
⫺ Not utilizable.
· Not known.
NUTRITIONAL REQUIREMENTS 77
PLANT
STEROLS
HO HO HO HO
desmosterol
HO
STRUCTURAL
COMPONENT OF
cholesterol TISSUES
HO
7 - dehydrocholesterol
HO
OH OH
OH
OH OH
MOLTING
HO HO HORMONES
OH OH
HO HO
H H
O O
ecdysone 20-hydroxyecdysone
Fig. 4.4. Metabolic pathways by which plant sterols are changed to cholesterol and the molting hormones in phytophagous
insects. Many intermediate steps are omitted.
have structural roles. Biotin, for example, is a component Lipogenic compounds Myo-inositol and choline are
of the enzyme pyruvate carboxylase in honeybees and constituents of some phospholipids, the phosphatidylinos-
probably in other insect taxa (Tu & Hagedorn, 1992). Folic itols and phosphatidylcholines (or lecithins), respectively.
acid is necessary for nucleic acid biosynthesis. In these In this role they are required in much larger amounts than
capacities, the vitamins can be spared, biotin by oleic acid vitamins, although in small quantities compared with the
and folic acid by dietary nucleic acid. main dietary constituents.
Some insects are known to have requirements for other Phosphatidylcholines are the major phospholipids in
B vitamins, in addition to the usual seven. For example, all insects except Diptera, and a dietary source of choline is
Tenebrio needs an external source of carnitine. probably necessary for all insects. In Drosophila, choline has
78 NUTRITION
a) consumption of high
100 protein diet 0.1
sucrose
consumption (%)
75
0 0
3 4 5 6
larval stage 0.05 protein
b) protein utilization
+
80 0 +
0 10 20 30
70 days
utilization (%)
female
Fig. 4.7. Changes in consumption and utilization of protein in oviposition. In anautogenous blowflies, such as Phormia,
successive larval stages of the gypsy moth, Lymantria. (a) The the intake of protein declines in the later stages of
percentage of the high protein diet eaten by each stage. Relatively vitellogenesis and then rises again after oviposition (Fig.
less of this diet was eaten by the later stages. Insects were given a 4.8). The intake of sugar may remain more or less con-
choice of two artificial diets. One contained high concentrations stant, but sometimes varies inversely with protein intake
of both protein and lipid, the other contained a low protein (de Clerk & de Loof, 1983). Similar changes may occur in
concentration with high lipid. Females have six larval stages, grasshoppers.
males only five (data from Stockhoff, 1993). (b) The efficiency of
Reviews: Barton Browne, 1995 – changes during development;
utilization of ingested protein declines in the later stages (after
Simpson & Simpson, 1990 – changes due to previous feeding
Montgomery, 1982).
an even stronger preference for the grains, but males lose 4.2.2 Maintaining a balance
this preference and accept leaves and grain with equal Many insects are known to select a diet which approxi-
readiness (Boys, 1978). mates an optimal balance of the major components. An
Some female mosquitoes do not lay eggs until they have insect can respond to a dietary imbalance in one of three
had their first blood meal; they are said to be anautogenous. ways. It can adjust the total amount ingested so that it
Others are autogenous and can lay their first batch of eggs acquires enough of the most limiting nutrient; it can move
without a blood meal. The protein for yolk production in from one food to another with a different nutrient balance;
autogenous mosquitoes comes from storage proteins and or it can adjust the efficiency with which it uses nutrients.
from the degeneration of flight muscles. Anautogenous Most of our understanding of dietary regulation by insects
mosquitoes obtain most of their protein from vertebrate comes from laboratory experiments using artificial diets.
blood. Each subsequent cycle of oogenesis is dependent on These experiments leave no doubt that insects do have the
a blood meal in both autogenous and anautogenous species. ability to achieve some degree of nutritional balance by
Cycles of varying nutrient intake may also occur in regulating food intake, and there is every reason to suppose
other species that exhibit discrete cycles of oogenesis and that this also occurs naturally, although the complex
BALANCE OF NUTRIENTS 81
weight (mg)
been shown to increase the amount eaten if the entire weight gain
nutrient composition of a diet is diluted with some inert 500
non-nutritional substance (see Wheeler & Slansky, 1991).
Melanoplus sanguinipes, feeding on dried wheat sprouts, 250
was able to maintain its intake of wheat close to optimal
even when the food was diluted 7:1 with cellulose. This 0
necessitated an almost 7-fold increase in the total amount
0 25 50 75 100
of food consumed (Fig. 4.9a). At the greatest dilution, the wheat in food (%)
insects were unable to compensate. Caterpillars of
Spodoptera compensated for dilution of the nutrients in
b) caterpillar
their diet from 30 to 10% by eating three times as much
(Fig. 4.9b). total consumption
Insects can also compensate for deficiencies in a class of 600 nutrients consumed
major nutrients by adjusting the total amount eaten. weight gain
Aphids feeding on artificial diets with different concentra- weight (mg) 400
tions of amino acids increased their intake on the more
dilute diets and were able to maintain their intake of amino 200
acids at similar levels (Fig. 4.10) (Prosser, Simpson &
Douglas, 1992). Locusts fed on artificial diets with either
0
high or low levels of protein ate more when confined to the
10 20 30
low protein diet. By contrast, they did not compensate for nutrients (%)
differences in the levels of carbohydrate, but compensation
for carbohydrates has been demonstrated in adult flies (For Fig. 4.9. Dietary compensation by insects with no choice of food.
example, Nestel, Galun & Friedman, 1985), in butterflies (a) A grasshopper, Melanoplus. Amount of food eaten in five days
by final stage larvae feeding on dried, ground wheat. The wheat
feeding on sugar solutions, and in cockroaches.
was mixed with indigestible cellulose in different proportions. On
If they have a choice of foods with different nutrient
all but the lowest concentration, wheat consumption and weight
levels, insects can regulate their nutrient intake by eating gain were almost constant because the insect ate more (data from
differentially from the foods available. In this way, grass- McGinnis & Kasting, 1967). (b) A caterpillar, Spodoptera.
hoppers and caterpillars can correct for a previous imbalance Amount of food eaten in the final larval stage. Nutrients were
of carbohydrate or protein (Fig. 4.11), and larval Heliothis are diluted with indigestible cellulose. Weight gain was similar
able to adjust the amounts of vitamins and lipids consumed. irrespective of the percentage of nutrients in the diet (data from
Given a choice of foods containing different amounts of inor- Wheeler & Slansky, 1991).
ganic salts, Locusta modifies its choice so that it maintains a
constant level of both salts and the major nutrients. In the excreted as uric acid or some other, unknown, nitrogenous
absence of a choice, however, different amounts of salts are end product of catabolism (Fig. 4.12) (Zanotto, Simpson &
ingested because the insect maintains the optimal intake of Raubenheimer, 1993). In Pieris, there is an inverse relation-
major nutrients (Trumper & Simpson, 1993). ship between the levels of particular amino acids in the diet
The importance of post-ingestive regulation of nutrient and the metabolic utilization of each amino acid, suggest-
balance is demonstrated by experiments with locusts. ing the presence of a mechanism regulating oxidation of
These insects maintained a relatively constant increase in specific amino acids according to needs (van Loon, 1988).
body nitrogen despite a more than 3-fold increase in the The ability to adjust food intake to nutritional require-
amount of nitrogen ingested. Very little of the protein was ments implies some feedback of nutritional status on food
present unchanged in the feces. Most of the excess was selection and feeding behavior. In the locust, feedback has
82 NUTRITION
a) total volume ingested back on its own nutrient status. Visual characteristics, odor
0.9 and taste due to chemicals other than the nutrients may
provide the stimuli and the association may be positive,
volume ingested (µl)
locust caterpillar
20
10
5
0 0
PC P C 0 PC P C 0
previous diet previous diet
protein carbohydrate
Fig. 4.11. Dietary compensation by insects with a choice of foods. Insects were given a choice of artificial diet containing
either protein or carbohydrate after a period of four hours during which only one of four different diets was available. The
previous diets contained protein and carbohydrate (PC), protein with no carbohydrate (P), carbohydrate with no protein (C),
or neither of these components (0). After feeding on PC, little feeding occurred; after 0, carbohydrate and protein were almost
equally acceptable. After feeding on P, the insects selected carbohydrate, and after feeding on C, they selected protein. The
histogram for the locust shows the amounts eaten in one hour, that for the caterpillar, the amounts eaten in eight hours (after
Simpson, Simmonds & Blaney, 1988).
amino acid
injection
(
a) b)
-40
0 30 60 90 30 60 90
time from end of meal (min) time from end of meal (min)
Fig. 4.13. Mechanism of diet regulation in larvae of Locusta . (a) changes in the total concentration of amino acids in the
hemolymph following the end of a meal (time 0) on artificial diet (after Abisgold & Simpson, 1987). (b) An experiment
showing the effects of increased amino acid concentration in the hemolymph on the firing rates of contact chemoreceptors on
the maxillary palps. Forty-five minutes after ending a meal the insects were injected with a cocktail of amino acids to simulate
the effects of feeding. The same sensilla were tested at intervals with sucrose, NaCl or a cocktail of amino acids. The
responsiveness to sucrose and salt declined slightly, but the sensitivity to amino acids was greatly reduced (after Abisgold &
Simpson, 1988).
associations are not species-specific. Several fungus genera Reviews: Beaver, 1989 – bark and ambrosia beetles; Bissett &
are associated with ambrosia beetles. Two of the best Borkent, 1988 – gall flies; Cherrett, Powell & Stradling, 1989 –
known are Fusarium and Ambrosiella. Most of those associ- leaf-cutting ants; Wood & Thomas, 1989 – termites
ated with bark beetles are in the genus Ceratocystis.
Leaf-cutting ants (Attini) are dependent on specific 4.3.2 Endosymbionts
fungi for larval food. Worker ants cut leaves, and other
parts, from living plants and carry them to the nest. Here, Many insects have micro-organisms extracellularly in the
the ants chew the plant fragments, removing the waxy gut lumen or intracellularly in various tissues.
cuticle and possibly also removing existing micro-organ-
isms on the plant surface. Using feces, they build the 4.3.2.1 Micro-organisms in the alimentary canal
chewed fragments into a garden which they inoculate with Micro-organisms are almost inevitably ingested during
hyphae from an existing garden. The fungi are feeding and so an intestinal flora is present in most insects.
Basidiomycetes that only occur in the nests of these ants. The alimentary canal of grasshoppers, for instance, is
Macrotermitinae also cultivate fungi in gardens, called sterile when the insect hatches from the egg, but soon
fungus combs, constructed from fresh fecal material con- acquires a bacterial flora which increases in numbers and
taining wood fragments. The fungus, in the genus species throughout life. In general, insects with straight
Termitomyces, is only found associated with termites. It alimentary canals contain fewer micro-organisms than
breaks down cellulose and lignin and, when ingested by the those with complicated guts which have a range of
termites, it contributes its cellulolytic enzymes to those of different pH values, providing a number of different
the insect. Nitrogen is also concentrated. In reproductive niches. The micro-organisms occurring in the gut in these
structures of the fungus, which are eaten by the termites, it cases of casual infection largely reflect what is present in
reaches 8% dry weight; the wood initially ingested may the environment (Brooks, 1963). At least in the case of the
have only about 0.3% dry weight. Termitidae, including locust, Schistocerca, and larval fruit flies, Rhagoletis, the gut
the Macrotermitinae, do not have endosymbiotic proto- flora does not contribute to the nutrition of the insect
zoa, unlike all the other termites. (Charnley, Hunt & Dillon, 1985; Howard & Bush, 1989).
FEEDING ON NUTRITIONALLY POOR SUBSTRATES 85
Table 4.3. Insects feeding on nutritionally poor diets and their associated symbiotic organisms
Micro-organisms
Wood Blattodea
Cryptocercus Hindgut Flagellates Cellulose digestion
Isoptera
Kalotermitidae Hindgut Flagellates Cellulose digestion
Hindgut Bacteria Nitrogen fixation
Macrotermitinae Ectosymbionts Fungi Cellulose digestion
Concentration of nitrogen
Coleoptera
Anobiidae Midgut cecal Yeasts Essential amino acids
epithelium
Scolytinae Ectosymbionts Fungus Concentration of nitrogen
Platypodidae Ectosymbionts Fungus Concentration of nitrogen,
sterols
Hindgut Bacteria Nitrogen fixation
Hymenoptera
Siricidae Ectosymbionts Fungus Cellulose digestion
Phloem Homoptera
Aphididae Hemocoel Bacteria Amino acids
Delphacidae Hemocoel Bacteria, Amino acids, sterols
yeasts
Adult tephritid flies have a dorsal diverticulum of the In other cases, it is known that micro-organisms in the
esophagus in which bacteria accumulate. In general, the gut contribute to the insect’s nutrition. Detritus-feeding
species of bacteria present reflect what is present on the cockroaches, such as Periplaneta, and crickets have bacteria
surface of host fruit, although some species do occur con- in the hindgut. They may be attached to projections from
sistently and in greater abundance than others (Drew & the intima of the hindgut and they enhance the insects’
Lloyd, 1987). It is not known if these bacteria are true sym- ability to digest plant polysaccharides, such as xylans,
bionts, or if they contribute to the nutrition of the flies. pectins and gums, and oligosaccharides, such as raffinose.
86 NUTRITION
cellulose
pectin
xylan
raffinose
bean gum
a) b)
15 80
volume (mm 3 x 10 -5 )
apterae
60
10
number
apterae
40
5 alatae alatae
20
0 0
0 5 10 15 0 10 20
Time (days) Time (days)
Fig. 4.15. Changes in the mycetocytes of the aphid, Megoura (after Douglas & Dixon, 1987). (a) Changes in the total volume
of mycetocytes in an individual. The insects become adult on about day 8 and begin to produce young on day 10. (b) Changes
in the numbers of mycetocytes in an individual aphid.
feeding on feathers and skin debris of birds, also have form organs known as mycetomes, often in the hemocoel.
mycetocyte micro-organisms. Micro-organisms in myce- Amongst holometabolous insects and some Homoptera, a
tocytes are also found in all cockroaches in the family mycetome is often only present in the larval stages. At
Blattidae and ants of the tribe Camponoti. These are metamorphosis it fragments into mycetocytes which
omnivorous insects, but it is suggested that their diet is become lodged in adult organs. The larval mycetome of
often poor with an imbalance of amino acids. the beetle Calandra is a U-shaped structure below the
foregut, but not connected to it; in the adult, mycetomes
Types of micro-organism The mycetocyte micro-organ- are present in the epithelium of the midgut ceca. In
isms of aphids and weevils are bacteria (Campbell, Bragg Hippoboscidae and Glossinidae, the mycetome is present
& Turner, 1992) and this is probably also true of the myce- as a discrete zone in the midgut epithelium.
tocyte micro-organisms in a majority of other insects. Mycetocytes generally do not divide; they increase in
Yeasts are present in Fulgoridae and Laodelphax amongst size, and endomitotic divisions lead to polyploidy. During
the Homoptera and in Anobiidae and Cerambycidae the larval and early adult period of aphids, individual cells
amongst wood-boring beetles. In Triatominae the micro- may increase in volume about 10-fold in apterous (wing-
organisms are Actinomycetes. less) morphs, but to a lesser extent in alates (winged
In general, only one form of micro-organism is found forms). The biomass of symbionts increases in parallel
in each insect species, but this is not true in many with the volume of the cells (Fig. 4.15). In alates, the
Homoptera. All Auchenorrhyncha appear to house more number of mycetocytes declines sharply when the insects
than one type of micro-organism and, in Fulgoridae, both become adult, but, in apterous individuals, this sharp
yeasts and bacteria are present. Some species have as many decline is delayed (Douglas & Dixon, 1987). It is not
as six different symbionts. Many aphid species have only a known how these changes are regulated.
single bacterial symbiont, but others may have two or three Within the mycetocytes of most insects, each micro-
different types; some also have yeasts. organism is in a separate vacuole surrounded by
membrane, but in Glossina and ants the symbionts are free
Location in the insect body Mycetocytes are large poly- in the cytoplasm.
ploid cells. They are scattered amongst the principal cells
of the midgut epithelium in Haematopinus (Anoplura), Roles of mycetocyte micro-organisms These micro-
while in cockroaches they are scattered through the fat organisms sometimes have a key role in the nitrogen
body. In other insects, the mycetocytes are aggregated to economy of their host insects. In Blattidae they recycle
88 NUTRITION
weight (µg)
artificial diet. Diet A contained a well-
200 200 balanced mixture of amino acids. The
aphids grew equally well irrespective
100 100
of the proportion of essential amino
0 0
acids and irrespective of the presence
20 35 50 20 35 50 of symbionts. Diet B contained a
essential amino acids (%) essential amino acids (%) mixture of amino acids in proportions
approximating those in the phloem of
normal no symbionts
Vicia, a normal host plant. Growth
b) sterols
was reduced in the absence of
development time number of offspring symbionts and was most markedly
15
20 affected at the lowest level of essential
amino acids (after Prosser & Douglas,
time (days)
waste nitrogen. Cockroaches do not excrete uric acid, they There is no general agreement about the ability of the
store it in cells in the fat body. These stores become bacterial symbionts of Homoptera to produce sterols.
depleted if the insect feeds on a diet low in nitrogen. The Experiments in which the symbionts are removed from the
symbionts can synthesize a range of essential amino acids, insects, as in the experiment with aphids shown in Fig.
including those containing sulfur. 4.16b, may be interpreted as indicating that sterols are
The symbionts of aphids and the beetle Stegobium are normally supplied by the symbionts. However, other bac-
known to upgrade non-essential amino acids to essential teria in the same group as those found in aphids are inca-
amino acids. The symbionts of Acyrthosiphon contribute to pable of producing sterols (see Campbell, 1989). It is,
the insect’s ability to survive on diets containing low levels however, possible that the yeasts associated with some
of essential amino acids, as is generally the case with aphids, planthoppers and the beetle, Lasioderma, do
phloem. Essential acids usually comprise less than 25% of produce sterols.
the total amino acid concentration in phloem, and some There is evidence that the symbionts of Anoplura and
essential amino acids may constitute less than 0.2 mol % of some beetles produce some of the B vitamins.
the total. The symbionts of Acyrthosiphon are of little
importance on a high quality diet, but are most effective 4.3.3 Transmission between generations
when the balance of amino acids approximates that occur- In view of the constant associations of specific symbionts
ring in the phloem of Vicia, a normal host of this aphid with particular insects and their obvious importance to the
(Fig. 4.16a) (Prosser & Douglas, 1992). insects, even though the details may not be known, it is to
NUTRITIONAL EFFECTS ON GROWTH AND DEVELOPMENT 89
15
10
b) adult weight
900 Fig. 4.19. Effects of food quality on size and number of larval
stages. Larvae of Spodoptera exempta were fed on one of three
different grasses which varied in their suitability for growth. On
weight (mg)
800 the two less favorable grasses the insects grew more slowly, but
they developed through one or two additional stages so that their
final sizes were similar. Head width is a measure of larval size
700 (data from Yarro, 1985).
600
0 0.25 0.5 1 ad lib
weight of food (mg/day)
yellow with a rough cuticle, and have two rows of reddish differences result entirely from differences in the quality of
spots along the midline. Caterpillars of the summer brood food eaten by the insects (Greene, 1989).
resemble stems. They are green-grey and are without the In the honeybee, the quality of food given to larvae by
rows of spots. They feed on leaves and have larger head the workers determines whether the larvae will become
capsules and mandibles than the spring brood. These queens or workers (section 15.5).
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Locusta migratoria and Spodoptera lit- inferred from fatty acid compositions Werren, J.H. (1997). Biology of
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biological significance of Steroids. In Comprehensive Insect armyworm (Spodoptera frugiperda)
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45–97. Lincoln: University of Trumper, S. & Simpson, S.J. (1993). mutualistic association between
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Stanley-Samuelson, D.W., Jensen, E., bee and some properties of related (Lepidoptera: Noctuidae) at constant
Nickerson, K.W., Tiebel, K., Ogg, biotin-containing proteins in other temperature and humidity conditions.
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5 Circulatory system, blood and immune systems
[94]
CIRCULATORY SYSTEM 95
Fig. 5.3. Functioning of incurrent ostia. (a) In the larva of Chaoborus. The valves are
prevented from opening outwards at systole by a unicellular thread (not shown) attached to the
inside of the heart (after Wigglesworth, 1972). (b) In the larva of Bombyx. The heart is shown
in horizontal (left) and transverse (right) sections.
nymphs; adults have two thoracic pairs in addition. running round the body wall from the segmental ganglia.
Mantids have only abdominal vessels. At the origin of each In Odonata, Blattodea, Phasmatodea, Orthoptera, larval
vessel from the heart, there is a muscular valve which Lepidoptera and some adult Coleoptera, branches of the
permits only the outward flow of blood. The walls of the segmental nerves combine to form a lateral cardiac nerve
vessels are non-muscular. running along each side of the heart. In Locusta, for
example, groups of neurons with cell bodies in the midline
Innervation The dorsal vessel of some insects, such as the in each abdominal ganglion send axons to the heart (Ferber
adult mosquito, Anopheles, lacks any innervation, although & Pflüger, 1990). In addition, a pair of neurosecretory cells
there are segmental nerves to the alary muscles. In most in the subesophageal ganglion each sends one axon
insect species, however, the heart is innervated by nerves forwards into the circumesophageal connective and
CIRCULATORY SYSTEM 97
cuticle a)
epidermis
suspensory
pericardial cells
sinus heart aorta
segmental
vessel
pericardial trachea
cells
perivisceral dorsal
sinus diaphragm
heart
excurrent
ostium
system, but lie adjacent to the heart itself. They are called epidermis muscle
5.1.1.2 Alary muscles and dorsal diaphragm Fig. 5.5. Dorsal and segmental vessels of the cockroach, Blaberus
The dorsal diaphragm is a fenestrated connective tissue (after Nutting, 1951). (a) Ventral dissection. The dorsal
membrane. It is usually incomplete laterally, so that the diaphragm is continuous over the ventral wall of the heart, but is
omitted from the drawing for clarity. Arrows show positions of
pericardial sinus above it is broadly continuous with the
incurrent ostia. (b) Transverse section through the pericardial
perivisceral sinus below. The lateral limits of the
sinus showing a segmental vessel arising from the heart and
diaphragm are indefinite and are determined by the pres- discharging into the hemolymph amongst the fat body laterally.
ence of muscles, tracheae or the origins of the alary (or
aliform) muscles which form an integral part of the origin is contractile, the rest, and greater part, being made
diaphragm. The alary muscles stretch from one side of the up of bundles of connective tissue which branch and anas-
body to the other just below the heart or, as in the cecropia tomose. Some of the connective tissue fibers form a plexus
moth, Hyalophora, are directly connected to the heart which extends to the heart wall. Orthopteroids may have as
muscles by intercalated discs. They usually fan out from a many as ten abdominal and two thoracic pairs of alary
restricted point of origin on the tergum and meet in a muscles, but in other insects the number is reduced. Most
broad zone in the midline (Fig. 5.2a), but sometimes, as in terrestrial Heteroptera, for instance, have from four to
grasshoppers, the origin of the muscles is also broad. In seven pairs. The alary muscles are visceral muscles with
most orthopteroids, at least, only the part near the point of 10–12 thin filaments to every thick filament.
98 CIRCULATORY SYSTEM, BLOOD AND IMMUNE SYSTEMS
5.1.1.3 Ventral diaphragm time, the volume of the subscutellar reservoir is increased
The ventral diaphragm is a horizontal septum just above and blood is drawn from the wings. When the muscles
the nerve cord cutting off the perineural sinus from the relax, the elastic ligaments restore the shape of the ampulla
main perivisceral sinus (Fig. 5.1). It is present in both so that blood is sucked into it from the reservoir.
larvae and adults of Odonata, Blattodea, Orthoptera, Most holometabolous insects, as well as Hemiptera,
Neuroptera (lacewings) and Hymenoptera, but is only have wing pulsatile organs in which a muscular
found in adults of Mecoptera (scorpion flies), Lepidoptera diaphragm, independent of the heart, bounds the sub-
and nematocerous Diptera. In Lepidoptera, it is unusual scutellar reservoir on the ventral side. It is suspended from
in having the nerve cord attached to its ventral surface by the scutellum by a number of filamentous strands (Fig.
connective tissue. When present, the diaphragm is usually 5.6a–c). Contraction of the muscles, which are innervated
restricted to the abdomen, but it extends into the thorax in from the ventral nerve cord, causes the diaphragm to
some grasshoppers and Hymenoptera. flatten, drawing blood from the wings. Relaxation of the
The structure of the diaphragm varies. For instance, in muscles is associated with an upward movement of the
the thorax of grasshoppers it is a delicate membrane with diaphragm, presumably due to the elasticity of the suspen-
little or no muscle, but in the abdomen it becomes a solid sory strands, and blood is forced into the body cavity (Fig.
muscular sheet. Laterally it is attached to the sternites, 5.6b,c).
usually at one point in each segment and so there are broad A pulsatile organ is also found at the base of each
gaps along the margins where perivisceral and perineural antenna. It consists of an ampulla from which a fine tube
sinuses are continuous. Its structure may vary with extends almost to the tip of the antenna. The ampullae of
developmental stage. For example, in Corydalis Thysanura (silverfish), Archaeognatha (bristletails) and
(Neuroptera) it forms a solid sheet in the larva, but a fenes- some Plecoptera have no muscles and it is presumed that in
trated membrane in the adult. these insects the ampulla serves simply to direct the flow of
Review: Richards, 1963 hemolymph from the opening of the aorta into the
antenna. In most insects, however, the ampullae have
5.1.1.4 Accessory pulsatile organs dilator muscles. Compression, which drives hemolymph
In addition to the dorsal vessel, insects have other pulsating into the antenna, results from the activity of elastic
structures that maintain circulation through the append- filaments on both sides of the wall of the ampulla. Only
ages. A pulsatile organ drawing blood from the wings is Dermaptera (earwigs) have compressor muscles.
present in both wing-bearing segments of most adult Periplaneta has a single muscle connecting the two ampul-
insects, but only in the mesothorax of Diptera and lae so that when it contracts both ampullae are dilated and
Coleoptera Polyphaga. A blood space, or reservoir, beneath hemolymph flows into each one through an ostium (Fig.
the posterior part of the tergum (scutellum) which is 5.6e–g). The contractions are myogenic in origin, but may
largely or completely isolated from the remaining hemo- be modulated by neural input since nerve endings do occur
coel of the thorax connects with the posterior veins of the on the muscle. However, most of the nerve endings are
wing via the axillary cord of the wing (see Fig. 5.8). The concentrated in the ampulla which appears to function as a
ventral wall of the reservoir forms a muscular pump. It may neurohemal organ. The axons originate in the sub-
be derived from the heart or it may be a separate structure. esophageal ganglion from a dorsal unpaired median
In hemimetabolous groups, other than Hemiptera, and neuron (section 10.3.2.4) and from a pair of somata placed
in Coleoptera and Hymenoptera Symphyta, the wing pul- laterally. Octopamine, probably from the dorsal unpaired
satile organ is an expansion or diverticulum of the dorsal median neuron, is present in the neurohemal area, but its
vessel with a pair of incurrent ostia opening from the sub- function relative to the ampulla of the antenna is not
scutellar reservoir. Odonata, for example, have, in each known. In Lepidoptera, the aorta ends anteriorly in a sac
pterothoracic segment, an ampulla which connects with from which the antennal vessels arise (see Fig. 5.7d).
the aorta by a narrow vessel (Fig. 5.6d). It is suspended Most insects have a longitudinal septum in the legs
from the tergum by elastic ligaments, and its dorsal wall is which divides the lumen into two sinuses and permits a
muscular. When the muscles contract, the ampulla is com- bidirectional flow of blood within the leg (see below). In
pressed and blood is driven into the aorta. At the same Hemiptera, the septum twists through 90 ° at the proximal
Fig. 5.6. Accessory pulsatile organs. In all diagrams, arrows indicate the direction of blood flow. (a)–(c) Wing heart not connected to the
aorta, such as occurs in most holometabolous insects. (a) Transverse section through the thorax showing the connection of the
subscutellar reservoir to the axillary cord of the wing. (b), (c) Diagrammatic longitudinal section, anterior to left. When muscles of the
diaphragm contract (b), the diaphragm is flattened and blood is drawn in from the wing. When the muscles relax (c), elastic suspensory
elements draw the diaphragm up and force blood out anteriorly (after Krenn & Pass, 1993). (d) Wing heart connected to the aorta as in
most hemimetabolous insects. Longitudinal section of the thorax. The subscutellar reservoir connects with the axillary cord of the wing
on either side (modified after Whedon, 1938). (e)–(g) Antennal pulsatile organ of cockroach. (e) General arrangement as seen from
above. Top of head cut away and brain removed. (f) Dilator muscle contracts, enlarging lumen of ampulla so that blood is drawn in from
the hemocoel in the head. Lowered pressure causes constriction at the origin of the antennal vessel so that the backflow of blood from the
antenna is restricted. (g) the muscle relaxes and the ampulla is flattened by the elasticity of its inner wall and the pull of the tendon. The
ostium is closed by a valve and blood forced into the antennal vessel (after Pass, 1985). (h) Leg pulsatile organ of Triatoma. Contraction of
the muscle compresses the blood sinus on one side of the septum and enlarges that on the other so that blood flows down the leg on one
side of the septum and up on the other (after Kaufman & Davey, 1971).
100 CIRCULATORY SYSTEM, BLOOD AND IMMUNE SYSTEMS
end of the tibia, and there is a muscle at this point (Fig. anterior
5.6h). When the muscle contracts, it compresses one sinus, from sinus
perivisceral C
forcing hemolymph into the thorax, and at the same time sinus
enlarges the other so that hemolymph is drawn into the leg. Sc
R+M
Its activity is probably myogenic although it may also be
subject to neural modulation (Hantschk, 1991). Cu
Some insects have very long cerci in which the mainte- post cubitus
nance of blood flow might require some special feature.
anal veins
Ephemeroptera have small, non-contractile vessels
extending from the posterior end of the heart into the
tergum wing
cerci. Plecoptera also have cercal blood vessels, but these
to perivisceral membrane
do not connect with the heart. They open directly into the sinus
perivisceral cavity, but the remainder of the cercal lumen
connects with the perivisceral cavity via the lumen of the to pulsatile
organ
paraproct. Changes in the volume of the paraproct pro- axillary cord
duced by a small muscle draw blood from the outer lumen
Fig. 5.8. Blood circulation in the base of the forewing of Blattella.
of the cercus and pump it into the perivisceral cavity. This
Areas in which the two membranes of the wing are fused together
flow draws blood into the cercus through the central vessel
are shaded. Well-defined channels, such as veins, are outlined by a
(Pass, 1987). solid line, less definite channels have no lines. Axillary sclerites
The muscle fibers in these different types of pulsatile are omitted (after Clare & Tauber, 1942).
organs generally have the characteristics of slow-contract-
ing muscles. Diptera, and because the heartbeat exhibits periodic rever-
Reviews: Krenn & Pass, 1994, 1995 – wing pulsatile organs; Pass, sals. As the abdomen contracts, the heart pumps blood for-
1991 – antennal pulsatile organs wards into the head (Fig. 5.7d). When the heart reverses, the
abdomen actively expands, drawing blood past the barrier of
5.1.2 Circulation fat (Fig. 5.7e). Movements of the hemolymph are coordi-
5.1.2.1 Movement of the blood nated with ventilatory movements (Wasserthal, 1982a). Any
During normal circulation of hemimetabolous and larval activity which tends to induce pressure differences between
holometabolous insects, the blood is pumped forwards different parts of the body must affect the circulation, and,
through the heart at systole, entering the perivisceral especially in adult Lepidoptera, Coleoptera and Diptera,
sinus through the anterior opening of the aorta in the head there is a close functional link between ventilatory and
and through the excurrent ostia where these exist. The hemolymph movements (see Figs. 5.10, 17.15).
valves on the incurrent ostia prevent the escape of blood Many insects appear to have a well-defined, but vari-
through these openings. The force of blood leaving the able circulation through the wings, although in some,
aorta anteriorly tends to push blood backwards in the apparently, circulation only occurs in the young adult. In
perivisceral sinus. The backwards flow is aided by the the absence of this wing circulation, the tracheae in the
movements of the dorsal diaphragm and by the inflow of wings collapse, and the wing structure becomes brittle and
blood into the heart, through the incurrent ostia, at dias- dry. In most cases, blood is drawn out of the wings from the
tole (Fig. 5.7a–c). Movements of the ventral diaphragm axillary cords by the thoracic pulsatile organs. In the
presumably help to maintain the supply of blood to the German cockroach, Blattella, the anal veins connect with
ventral nerve cord. the axillary cord through channels between the upper and
In adult Lepidoptera, Coleoptera and Diptera, and lower wing membranes. As blood is drawn out posteriorly,
perhaps in some other insects, the blood is shunted back- it is drawn in anteriorly from a blood sinus from which the
wards and forwards between the thorax and abdomen, major anterior veins arise (Fig. 5.8).
rather than circulated. This is possible because the hemo- A different mechanism has been described in a number
coel in the two parts is separated by a moveable flap of fatty of Lepidoptera. Here, the blood enters the wings along all
tissue, in Lepidoptera, or large airsacs, in cyclorrhaphous the veins (Fig. 5.9) while the heart is beating forwards and
102 CIRCULATORY SYSTEM, BLOOD AND IMMUNE SYSTEMS
ebbs out again during heartbeat reversal. The wing pul- In insects lacking leg pulsatile organs, the flow of blood
satile organs are active when the heart is beating backwards through the legs is thought to be maintained by pressure
(Fig. 5.10), so blood is drawn out of the wings and pushed differences at the base. Blood passes into the posterior
back into the abdomen. The movement of blood out of the compartment of the legs from the perineural sinus and out
veins causes the tracheae inside them to expand so that air into the perivisceral sinus from the anterior compartment.
is drawn into the wing. When the pulsatile organ stops and In Lepidoptera, blood flow in the legs is dependent on the
the heart starts beating forwards again, the negative pres- elasticity of the tracheae as described above for the wings
sure on the wing tracheae is removed and their elasticity (Wasserthal, 1982b).
causes them to contract. This produces a negative pressure The efficiency of this system, with respect to the rate at
in the hemolymph space outside the trachea and blood which substances are translocated round the body, may
flows in. This is only possible because of the specialized vary with the physiological state of the insect. Fluorescein
nature of the taenidia in the tracheae of the wings. The injected into the abdominal hemocoel of Periplaneta can
taenidial thickenings of typical tracheae function reach the pulvilli in four to eight minutes. Radiolabel from
specifically to prevent such changes in volume as occur in labelled sucrose was detected in the labial palps of Locusta
the tracheae of the wings, but in the giant silk moth, within five minutes of being eaten (including digestion and
Attacus, and presumably in other Lepidoptera, the taenidia absorption). Longer periods may be required for injected
of the wing tracheae are coiled along their length like a substances to be uniformly distributed through the hemo-
spring (Fig. 5.10c,d). Extension of the trachea induced by lymph, and this is affected by temperature. At 22–25 °C,
negative pressure outside stretches the taenidia. When the labelled material was uniformly distributed in the hemo-
negative pressure is removed, their spring-like properties lymph of the honeybee, Apis, within five minutes; at 12–14
cause them to resume their relaxed position, reducing the °C it required more than 15 minutes (Crailsheim, 1985).
volume of the trachea (Wasserthal, 1982a). A similar Some reports indicate that injected dyes may take more
system involving the reciprocal movement of blood and air than an hour to become uniformly distributed through the
into and from the wings probably occurs in Coleoptera, hemolymph. It is possible that, in these cases, the circula-
and possibly in other groups. tion was disrupted by wounding.
CIRCULATORY SYSTEM 103
presystolic
notch a) Bombyx
heartbeat (contractions.min -1 )
100
diastasis
diastole systole L2 L3 L4 L5 pupa adult
large 80
60
volume of heart
40
20
small 0
0 10 20 30 40 50
time
heartbeat (contractions.min -1 )
beating. The presystolic notch results from an increase in
hydrostatic pressure, producing a slight increase in volume 120 L 1 L 2 L 3 L 4 L5 adult
within this part of the heart due to the start of systole in the more
posterior segments. 100
5.1.2.2 Heartbeat 80
Systole, the contraction phase of the heartbeat, results from
the contractions of the intrinsic muscles of the heart wall. In 60
a majority of insects this activity begins posteriorly and 0 10 20 30 40 50
spreads forwards as a wave. In Periplaneta and Orthoptera, days
however, a synchronous contraction of the heart occurs Fig. 5.12. The frequency of heartbeat at different stages of
along its whole length. This type of action is probably asso- development. L1–L5 indicate larval stages; arrows indicate
ciated with the presence of excurrent ostia or segmental ecdysis. (a) In Bombyx (after Masera, 1933). (b) In Locusta (after
vessels. Even in these insects, peristaltic heart contractions Roussel, 1972).
may sometimes occur. Diastole, the expansion phase when
blood enters the heart, results from relaxation of the heart the last (Fig. 5.12a). In the pupa, the heartbeat falls to
muscles assisted by the elastic filaments that support the 10–20 per minute and remains at this low level until
heart. In general, the alary muscles are not responsible for shortly before adult eclosion. A similar, but slightly less
diastole and often contract at a lower frequency than the marked change occurs during the development of the
heart. In Rhodnius, however, complete diastole is dependent migratory locust, Locusta, but the rate of beating tends
on the alary muscles (Chiang et al., 1990). After diastole to rise before a molt (Fig. 5.12b). In Lepidoptera, a very
there is a third phase in the heart cycle known as diastasis in sharp increase in the heart rate occurs at eclosion, falling
which the heart remains in the expanded state (Fig. 5.11). to a sustained but moderate rate when eclosion is com-
Increases in the frequency of the heartbeat result from plete (Fig. 5.13).
reductions in the period of diastasis. In addition to these intrinsic changes, the rate of heart-
beat is affected by environmental factors. Activity usually
Rate of heartbeat The frequency with which the heart stops above 45–50 °C and below 1–5 °C. Within this range
contracts varies considerably both within and between the rate is higher at higher temperatures. In Locusta, the
species. In general, the frequency of beating is higher in rate of heartbeat is also higher in the light than in the dark.
early than in later stage larvae. It also depends on the age It is common for the heart to stop beating, sometimes
within a stage of development. For example, in silk- for a few seconds, but sometimes for 30 seconds or more.
worms (Bombyx), the rate drops from 80 beats per The heart of the young pupa of Anopheles sometimes stops
minute in second stage larvae to about 50 in the fifth beating altogether, and in old pupae no activity of the heart
stage, and it drops sharply just before each molt except is observed.
CIRCULATORY SYSTEM 105
250
200
175
hormone activity
(arbitrary units)
antidiuretic diuretic
activity activity
5.2 HEMOLYMPH
time (hours)
5.2.1 Hemolymph volume
The hemolymph volume, expressed as a percentage of the Fig. 5.15. Regulation of blood volume in relation to ecdysis in
Periplaneta (after Mills & Whitehead, 1970). (a) Changes in blood
total body weight of the insect, varies with the type of
volume. (b) Antidiuretic and diuretic activity of the hemolymph,
insect. In the heavily sclerotized tenebrionid beetle,
suggesting that changes in hormonal activity regulate the changes
Onymachus, blood constitutes about 11% of the beetle’s in volume.
total mass; in mid-stadium larvae of Locusta, the figure is
about 18%, while in mature adults it is about 12%; in
cockroaches it is about 17% and in caterpillars 35–40%. cabbage butterfly, Pieris, by about 70% in the hours follow-
Hemolymph water comprises 20–25% of the total ing eclosion (Nicolson, 1980a).
body water in adult insects, but in caterpillars, the figure is Hemolymph volume is also affected by other factors.
close to 50%. This reflects the important hydrostatic func- In Locusta, the hemolymph volume falls following
tion of the hemolymph in these larval forms. This role is feeding, apparently because water moves into the gut.
further evidenced in other insects at the time of the molt Volume changes also result from desiccation. In the
where an increase in hemolymph volume occurs before desert tenebrionid, Onymacris, hemolymph volume is
each ecdysis. Before each molt of the desert locust, reduced by about 60% after 12 days in desiccating condi-
Schistocerca, the relative blood volume almost doubles, and tions (Fig. 5.16c). Similar changes occur in even shorter
is then reduced again after the molt (Fig. 5.14). In periods under extreme environmental conditions. It is
Periplaneta, the pre-molt increase in volume is associated almost impossible to obtain blood samples from red
with an increase in activity of an antidiuretic hormone and locusts, Nomadacris, collected in the heat of the after-
the post-ecdysial fall in volume is produced by a transient noon, but the insects have ample blood in the morning
rise in the hemolymph titer of diuretic hormone (Fig. and late evening.
5.15). Diuresis reduces the hemolymph volume of the An important function of the hemolymph is to provide
HEMOLYMPH 107
Table 5.1. Major inorganic ions in the hemolymph of different insects (concentrations in mequiv l⫺1)
Notes:
(L), larva.
·, No data.
Food Na K Ca Mg
Order/species Larva Adult Larva Adult Larva Adult Larva Adult Larva Adult
Hymenoptera
Apis Brood food Nectar 214 251 ⬃38 29 ⬃23 19 2126 21
Vespula Insects Insects, fruit 221 280 ⬃45 12 ⬃15 21 2119 21
Lepidoptera
Mamestra Leaves Nectar 225 215 ⬃17 41 ⬃12 10 2163 34
Bombyx Leaves None 221 228 ⬃28 36 ⬃11 13 ⬃ 63 43
Hyalophora Leaves None 222 222 ⬃39 27 ⬃12 29 l 100 39
Coleoptera
Oryctes Detritus Detritus 228 245 ⬃14 29 ⬃28 29 2165 37
Timarcha Leaves Leaves 221 220.4 ⬃14 17 ⬃18 29 2166 74
Ergates Wood ? 213 222 ⬃19 12 ⬃27 27 2153 59
Diptera
Chironomus Plankton None 110 150 ⬃20 50 ⬃冢· 2· 22· 2·
Note:
·, No data.
110 CIRCULATORY SYSTEM, BLOOD AND IMMUNE SYSTEMS
alanine
aspartic acid
non-essential amino acids
cysteine/cystine
glutamic acid
glutamine
glycine
proline
serine
tyrosine
concentration (µM)
returns to its original level within about one hour, but, in a) Blatta - larval-specific protein
Rhodnius, feeding only once in each developmental stage, it 10
larva larva larva adult
remains constant through the period of molting. It appears 8 5 6 7
that the utilization of amino acids is offset by the slow, 6
continuous digestion of the blood meal in this insect.
4
single storage protein comprises about 60% of the soluble Leptinotarsa, enters diapause as an adult, while the pink
protein. Arylphorins are not produced after the bollworm, Pectinophora, diapauses as late stage larvae.
larva/pupa molt, but in some insects other proteins, such Both species accumulate proteins that are specific to the
as serum protein I in Blatta (Fig. 5.20b) are still present at diapause period (Koopmanschap, Lammers & de Kort,
high concentrations in the adult stage. Females of some 1992; Salama & Miller, 1992), but the functions of these
species produce more storage protein than males and some proteins are not known.
have a female-specific protein.
Rising ecdysone concentrations regulate the decline in Lipid transport proteins Because lipids are not soluble in
arylphorin mRNA before a molt (Fig. 5.20c), but a methio- water their transport through the hemolymph involves
nine-rich protein produced only in the final larval stage of combination with proteins to form lipoproteins. Insects
Manduca appears to be regulated by juvenile hormone have a single class of lipoprotein called lipophorins. The
inhibiting production of its mRNA. High concentrations major lipid components of lipophorin are diacylglycerides
of these proteins may persist in the hemolymph in the and phospholipids, although smaller amounts of tri-
absence of synthesis if they are not removed by the fat acylglycerides, fatty acids and cholesterol are present.
body. The lipid component is solubilized by the presence of two
At each molt, arylphorin is taken up into the fat body or three different proteins called apolipoproteins I, II and
where it is temporarily stored in granular form. Uptake III. Apolipoproteins I and II are always present;
may, in part, be unselective as there is a general turnover of apolipoprotein III is added in some species during periods
proteins at metamorphosis, but selective uptake of the of peak lipid movement through the hemolymph. The
storage protein also occurs. The bulk of the storage protein particles so produced vary in composition and density, the
appears to be broken down into its component amino acids more lipid present, the lower the density. High-density
in the fat body and forms the basis of tissues in the next lipophorin (HDLp) contains relatively little lipid; low-
developmental stage. Amino acids derived from larval density lipophorin (LDLp) has more lipid. HDLp and
storage protein occur in all adult tissues, but contribute LDLp are not discrete categories. Their densities can vary
especially to flight muscles and cuticle which, because of and particles with predominantly different densities may
their bulk, contain large amounts of protein. It is probable be present at one time. Very-high-density lipophorin
that storage proteins also contribute to yolk formation, (VHDL) is sometimes produced. The most common is
contributing the amino acid building blocks for vitel- vitellogenin.
logenin synthesis, and, in autogenous mosquitoes, they Fatty acids are transported in the hemolymph primar-
disappear from females as yolk synthesis begins. In queens ily as diacylglycerides. Diacylglycerides derived from the
of many ant species, the storage proteins persist for some food are taken up by HDLp at the hemolymph boundary
time after the nuptial flight and provide sufficient protein of the midgut epithelium. From here they are transported
for development of the first brood of workers, which, in to the tissues for utilization or, commonly, to the fat body
most species, takes place without the queen feeding for storage. The HDLp does not enter the cells but
(Wheeler & Buck, 1995). unloads the diacylglyceride at the cell wall and returns to
Despite the apparent importance of the storage pro- circulation. Within the fat body, fatty acids are stored
teins, mutants of Drosophila can survive for many genera- mainly as triacylglycerides so that their subsequent move-
tions without any larval serum protein I although this is ment to other tissues requires resynthesis of diacylglyc-
normally present in large amounts. Adult survival and erides (Fig. 5.21b). This occurs at the cell boundary and
longevity are not affected by its absence, but there is a then diacylglycerides are again loaded on to HDLp for
marked reduction in fecundity. This is largely due to a transport to the appropriate tissues.
failure of the flies to mature rather than any direct quanti- During normal metabolism the additional lipid added
tative effect of the protein, but it appears that oocyte to HDLp presumably makes only small changes to the
development may also be affected (Roberts, Turing & volume and density of the particle. However, when the
Loughlin, 1991). demand for lipids is high, as in adult Locusta and the
Specific proteins also accumulate in the hemolymph of tobacco hornworm, Manduca, both of which use lipids as
insects entering diapause. The Colorado potato beetle, the main fuel for flight, so much lipid is added to the
HEMOLYMPH 113
b)
100 100
sterol
75 75
monacylglycerol
diacylglycerol
%
50 50
triacylglycerol
25 25
0 0
fat body hemolymph
HDLp that its increasing size would result in a loss of hemolymph. Some lipophorin has only a low affinity for
solubility but for the addition of apolipoprotein III. The the hormone, but in some insects a separate lipophorin
larger, low density particle produced by this process is with high affinity for juvenile hormone is also present.
LDLp (Fig. 5.21a). The mobilization of lipid in the fat This serves not only to transport the hormone, but also to
body is controlled by adipokinetic hormone. At the flight protect it from the action of juvenile hormone esterase
muscle, the LDLp is unloaded and HDLp and (King & Tobe, 1993). Some insects have juvenile hormone
apolipoprotein III return to circulation. It is possible that binding proteins that are not lipophorins.
apolipoprotein III also becomes associated with HDLp in The apolipoproteins are synthesized in the fat body
larval Manduca when lipid demands are high (Ziegler et where they are combined with phospholipids and released
al., 1995). into the hemolymph as nascent lipophorin particles.
About 90% of the lipid that accumulates in the devel- Diacylglycerides are normally added at the gut epithelium.
oping oocytes of Manduca is transported as LDLp and the In Manduca larvae, apoprotein mRNA is present during
lipoprotein is recycled in the hemolymph. However, some the feeding stages and total lipophorin increases, but no
of the lipid is transported by vitellogenin and by another mRNA is available after feeding stops in each larval stage
VHDL. In this case, the lipoprotein is not recycled, but is although the amount of lipophorin remains constant (Fig.
retained in the oocyte. 5.22). Synthesis starts again in the pupal stage about 12
Juvenile hormone is transported by lipophorins in the hours before eclosion.
114 CIRCULATORY SYSTEM, BLOOD AND IMMUNE SYSTEMS
Organic acids are present in some quantity in the a) Orthoptera b) Neuroptera c) Lepidoptera
plasma. The major components are acids associated with
cations anions cations anions cations anions
the citric acid cycle, including citrate, ␣-ketoglutarate,
succinate and malate. Citrate is usually present in high
concentration, although this varies considerably from one
species to another. Organic phosphates are often present
in high concentrations and in some insects tyrosine is
present as a phosphate. This is an alternative to glycosyla-
tion as a means of achieving a high concentration of tyro-
sine.
Fig. 5.25. Different types of hemocyte (a) after Chiang, Gupta & Han, 1988; others after Rowley and Ratcliffe, 1981): (a)
prohemocyte of Blattella; (b) plasmatocyte of larval Galleria; (c) granulocyte of larval Galleria; (d) granulocyte (cystocyte) of
Clitumnus. Arrowheads indicate swollen perinuclear cisterna; (e) spherule cell of larval Galleria. The large open areas, looking
like vacuoles (and labelled V), are probably caused by extraction of spherules during preparation; (f) oenocytoid from larval
Galleria. Inset shows size of nucleus relative to whole cell.
Abbreviations: G, granules; GO, Golgi complex; IG, developing granules; M, mitochondria; MT, microtubules; MVB,
multivesicular body; N, nucleus; PE, protoplasmic extensions; PO, ribosomes; PV, pinocytotic vesicles; R, ribosomes; RER,
distended cisternae of rough endoplasmic reticulum; SP, spherules; V, vacuole.
HEMOLYMPH 117
a) b)
5 m
2 m
c) d)
1 m
5 m
e) f)
5 m
5 m
118 CIRCULATORY SYSTEM, BLOOD AND IMMUNE SYSTEMS
hemocytes (number.µl )
-1
from Arnold & Hinks, 1976). (a)
0
0 1 2 3 4 5 6
larval stage
Spherule cells are characterized by the large, refractile lack hemopoietic organs, new hemocytes can only be pro-
spherules which may occupy 90% of the cytoplasm. They duced in this way. This appears also to be the case during
are not usually very common although they are found in the larval stages of the milkweed bug, Oncopeltus.
most of the species studied. Their function is unknown. Elsewhere, hemocyte production from existing cells
Oenocytoids occur mainly in Lepidoptera where they appears to complement production in hemopoietic organs,
are amongst the largest of the hemocytes. These cells but where the hemopoietic organs persist in adult insects,
exhibit little development of rough endoplasmic reticulum as in Blattodea and Orthoptera, mitotic division of existing
or Golgi complexes, but they have a complex array of hemocytes is relatively rare.
microtubules and sometimes also crystalline inclusions. Not all types of cell divide and the rates of division vary
Their function is unknown. even amongst those that do. Between 0.2 and 0.4% of pro-
Adipohemocytes characteristically contain lipid droplets. hemocytes were found in division in blood samples taken
The nucleus: cytoplasm ratio is low, and they contain well- during the first four stages of larval development of the
developed endoplasmic reticulum and Golgi complexes. moth, Euxoa, but this level declined in the final larval stage
Reviews: Brehélin & Zachary, 1986; Gupta, 1979a, b, 1985, 1991; (Fig. 5.26a). Mitotic activity was similar in granulocytes,
Rowley & Ratcliffe, 1981 but amongst spherule cells it increased from zero in the
first two stages to about 0.25% in the final stage.
5.2.4.1 Origin of hemocytes Plasmatocytes only rarely divide in at least a majority of
Hemocytes are derived from the embryonic mesoderm. insects. Despite this, the number of plasmatocytes per unit
Subsequently, new hemocytes are produced by mitotic volume of hemolymph increases throughout larval
division of existing, circulating hemocytes, or from previ- development (Fig.5.26b). They are probably derived from
ously undifferentiated cells in structures known as hemo- the prohemocytes which remain constant in relative abun-
poietic organs. dance despite their high mitotic rate.
Much of the literature suggests that the mitotic rate for
Mitotic division of hemocytes The production of new all the cells only rarely exceeds 1%, but some work indi-
hemocytes by mitosis of existing blood cells is a wide- cates much higher rates. Arnold & Hinks (1983) suggest
spread phenomenon. In adult holometabolous insects that that in the final larval stage of Euxoa, the mitotic index of
HEMOLYMPH 119
spherule cells may exceed 10% (see caption to Fig. 5.26) process of hemopoiesis appears essentially similar in other
and in the final larval stage of the milkweed bug, insects although the reticular cells exist as aggregations
Oncopeltus, a mitotic index of 4% was recorded. with no bounding layer and, in Lepidoptera, reticular cells
On the basis of the mitotic activity of the cells, it is sug- are absent.
gested that the whole population of granulocytes in the last Reviews: Feir, 1979 – mitosis; Hoffmann et al., 1979 –
larval stage of Euxoa turns over in about 5 days; the hemopoietic organs
spherule cell population would turn over in less than one
day (Arnold & Hinks, 1983). Other estimates of hemocyte 5.2.4.2 Numbers of hemocytes
longevity, in Galleria, suggest that plasmatocytes survive Estimates of the total number of hemocytes in an insect
for at least nine days. show that small insects have many fewer hemocytes than
large insects. Adult female mosquitoes have a total of less
Hemopoietic organs Blood is formed in structures called than 10 000 hemocytes, whereas adult Periplaneta have
hemopoietic organs. Since, in insects, only the blood cells, more than 9 000 000. Similar trends occur within a species.
not the plasma, are produced in these structures, they Second stage caterpillars of Euxoa have about 4000 hemo-
should strictly be called hemocytopoietic organs, but the cytes; sixth stage larvae have about 2 400 000. The number
general term is more usual. Hemopoietic organs have been may also vary cyclically. For example, in the last stage larva
described in some Orthoptera, a blattid and a few larval of the wax moth, Galleria, the total number of cells is at
Lepidoptera, Diptera and Coleoptera. They persist in first constant at about 2.2 million and then increased to
adult Orthoptera, but not in adults of holometabolous almost 4 million before the insect molts (Fig. 5.28a). An
species. No hemopoietic organs are present at any stage of even bigger relative increase occurs during the postfeeding
the milkweed bug, Oncopeltus. stages of the final stage larva of Sarcophaga, but at the time
The positions of hemopoietic organs vary from species of pupariation, when the larva becomes immobile, there is
to species, but in most cases they are associated with, a sudden rapid decline (Fig. 5.29).
though not necessarily connected with, the heart. In the Increases in numbers of circulating cells may result
cricket, Gryllus, and the mole cricket, Gryllotalpa, they are from the production of new cells or, possibly, by the
paired, segmental structures on either side of the heart and recruitment of cells adhering to other tissues. Reduction in
opening into it (Fig. 5.2). In Locusta, Periplaneta, and larvae hemocyte number may result from cell death or from an
of cyclorrhaphous flies and of the beetle, Melolontha, they increase in the numbers adhering to the tissues.
consist of irregular accumulations of cells close to the Counts of the number of cells per unit volume of
heart, but not connected with it (Fig. 5.27a,b). By contrast, hemolymph (usually called the ‘total hemocyte count’)
in caterpillars they are groups of cells around the develop- may not reflect the total number of hemocytes in circula-
ing imaginal wing discs (Fig. 5.27c,d). tion because the blood volume varies. For example, in the
Only in the grylloids is the hemopoietic organ a dis- last stage larva of Galleria, when the total number of cells
crete structure bounded by a cell layer and with an ill- is constant (Fig 5.28, weight less than 200 mg) the
defined lumen opening into the heart. Even here, the number per unit volume decreases because the blood
bounding layer of cells is incomplete. Within this bound- volume is increasing. From a functional standpoint, such
ary are irregularly shaped reticular cells apparently as wound healing or combatting invaders, the number per
embedded in a connective tissue matrix. These cells unit volume may be more important than the total
undergo mitotic divisions and give rise to hemocyte stem number.
cells. By further division, the stem cells form clusters of The number of hemocytes per unit volume of blood
cells which differentiate synchronously to form hemo- tends to increase throughout larval development, but with
cytes. Granulocytes and plasmatocytes are formed in this additional variation within each developmental stage (Fig.
way. They separate from the cortical region and enter the 5.30). It reaches a maximum at the time of each ecdysis,
circulation, presumably via the heart. The reticular cells except the pupa/adult ecdysis. The lack of a peak at this
are also phagocytic, taking up foreign material from the time may reflect the fact that major restructuring of the
hemolymph. Because of this the hemopoietic organs in tissues occurs earlier in the pupal period. In hemimeta-
these insects were originally called phagocytic organs. The bolous insects, the numbers are generally similar in larval
120 CIRCULATORY SYSTEM, BLOOD AND IMMUNE SYSTEMS
and adult insects, but in holometabolous species it is usual Rhodnius, changes in relative abundance occur in relation
for larvae to have more cells per unit volume of blood than to feeding and molting.
adults. In general, adult females have a higher number of Review: Shapiro, 1979
hemocytes than males.
5.2.4.3 Functions of hemocytes
Hemocyte profile The relative abundance of different Hemocytes perform a variety of functions. Among the
types of hemocytes (called the hemocyte profile or a more obvious are wound repair and defense against
differential hemocyte count) is not constant. parasites and pathogens (see below), but they have roles in
Plasmatocytes and granulocytes are usually the most many aspects of the normal functioning of the insect.
abundant, often comprising more than 80% of the total Granulocytes and spherule cells of larval Calpodes syn-
hemocyte population (Figs. 5.26c, 5.29b). The relative thesize polypeptides which are secreted into the hemo-
abundance of plasmatocytes tends to decline, and that of lymph and subsequently incorporated into the cuticle.
granulocytes to increase, through the larval period, but a Other peptides produced by hemocytes are probably
sharp reversal occurs at pupariation in Sarcophaga when added to the basal lamina (Sass, Kiss & Locke, 1994).
the total hemocyte count drops. The relative numbers of The hemocytes contain many proteases some of which
other cell types also change; spherule cells virtually dis- appear to be involved in the breakdown of tissues at meta-
appear from the blood of Sarcophaga at pupariation. In morphosis. For example, some hemocytes of Sarcophaga
IMMUNITY 121
hemocytes (millions)
2
1.5
2
1
0.5
0 0
60
75
hemocytes (%)
plasmatocytes
40
50
20
25
spherule cells
0 0
0 1 2 3 4 5 6 7
days
c) hemocyte count
Fig. 5.29. Changes in the hemolymph during the last larval stage
50,000
of Sarcophaga (data from Jones, 1967): (a) total number of
hemocytes (number.µl-1)
25,000
release material which forms a gel. This gel is stabilized by
plasma lipophorins and phenoloxidases from the hemocytes
may also be important. It is not known what causes the cells
0 to move to the site and degranulate, but possibly some
150 175 200 225 injury factor is produced by damage to the basal lamina. On
weight (mg)
the other hand, in Calliphora, clotting involves the clump-
Fig. 5.28. Changes in the hemolymph during the last larval stage ing and interdigitation of hemocytes without gelation.
of Galleria (data from Shapiro, 1979): (a) total number of Some time after clotting has occurred, plasmatocytes
hemocytes; (b) blood volume; (c) hemocyte count per microliter migrate to the site (Fig. 5.31). In Rhodnius the cells become
of blood. linked to each other by zonulae adherens within 24 hours of
the wound occurring and subsequently tight junctions and
have a 200 kDa protein in the cell membrane. These cells septate desmosomes are formed. In this way, hemocytes
increase in number at the time of pupation and the 200 kDa become bound together to form a continuous tissue. The
protein binds to sites on the basal lamina of the fat body. epidermal cells migrate over the clot to repair the wound.
Here the cells release a cathepsin-type protease which dis-
sociates the fat body (Kurata, Saito & Natori, 1993).
5.3 IMMUNITY
If the epidermis is damaged, a blood clot forms beneath
the wound. Formation of the clot involves components Insects exhibit defensive responses when their tissues are
from both the hemocytes and the plasma. Granulocytes invaded by other organisms. These are now generally
122 CIRCULATORY SYSTEM, BLOOD AND IMMUNE SYSTEMS
plasmatocytes, although the effect is less marked. The produced during metamorphosis is also removed by
numbers of other types of hemocyte appear unaffected by phagocytosis.
the infection (Chain & Anderson, 1982). The reduction in Avoidance of phagocytosis by pathogenic organisms
plasmatocyte numbers may result from a greater tendency may depend on different mechanisms. For example,
for the hemocytes to adhere to other objects, either the hyphal bodies of the fungal pathogen Nomuraea, which is
insect’s own tissues or an invading organism. In the latter capable of killing armyworms, Spodoptera, are not phago-
instance this behavior is associated with nodule or capsule cytosed. Beauveria, another fungal pathogen which is less
formation and the sustained low hemocyte count associated virulent, is phagocytosed, but nevertheless a germ tube
with pathogenic bacteria is probably a further reflection of can develop and produce hyphae (Hung, Boucias & Vey,
this as more cells adhere to the capsule. An increased ten- 1993). It appears that the surface characteristics of the first
dency of hemocytes to bind to lectins following wounding are not distinguished as ‘foreign’ by the insect. Beauveria is
or infection by the fungus, Beauveria, has been demon- recognized, but possibly produces immunosuppressive
strated in the grasshopper (Fig. 5.32b). While the effect of factors which suppress the host’s immune response
wounding alone is short-lived, the fungus has a more sus- (section 5.3.4).
tained effect (Miranpuri & Khachatourians, 1993). It is also
probable that mortality of hemocytes is produced by toxins Nodule formation Large numbers of bacteria or fungal
secreted by the invading bacteria or fungi. spores are attacked in a different way, by the formation of
The response of the hemocytes in pupal Lepidoptera is nodules (Fig. 5.33). Within a few minutes of entry, bacteria
quite different. Here the number of cells increases ten-fold are found trapped in the coagulum produced by numbers
within an hour of wounding, and this elevated count is of granulocytes. In some insect species, melanization of
maintained for several days. the necrotic granulocytes and the coagulum begins within
five minutes. After about two hours, plasmatocytes arrive
Phagocytosis Small numbers of bacteria, fungal spores or and begin to form a layer round the outside of the clump of
protozoans are phagocytosed by plasmatocytes. Non- cells. Little phagocytosis occurs. The intensity of the
pathogenic and weakly pathogenic organisms are dealt response varies, depending on the pathogenicity of the
with effectively in this way, but the means by which they invading organisms. More strongly pathogenic organisms
are killed are not known. Possibly bactericidal proteins induce a stronger and more rapid response than non-path-
produced by the hemocyte are involved. Tissue debris ogenic forms (Ratcliffe & Walters, 1983). There is evidence
124 CIRCULATORY SYSTEM, BLOOD AND IMMUNE SYSTEMS
a) Galleria c) Orgyia
25 125
control
hemocytes (number.µl-1)
hemocytes (number.µl-1)
20 wounded 100 injected
control
15 75
10 50 Cotesia
5 Bacillus 25
0 0
0 6 12 18 24 0 6 12 18 24
b) Melanoplus d) Orgyia
Beauveria
hemocytes binding to lectin (%)
40
0 0
0 6 12 18 24 0 12 24 48 72 96
time (hours post parasitism or wounding) time (hours post parasitism or injection)
Fig. 5.32. Changes in hemocyte counts and binding properties due to wounding or infection. (a) Hemocyte count of larval
Galleria following wounding or infection by a pathogenic Bacillus (data from Ratcliffe & Walters, 1983). (b) Binding
properties of hemocytes of the grasshopper, Melanoplus, following wounding or infection by the fungus, Beauveria (data
from Miranpuri & Khachatourians, 1983). (c) Hemocyte count of larval Orgyia following parasitism by the wasp Cotesia,
or injection of a mixture of venom and the contents of the calyces of the wasp (after Guzo & Stoltz, 1987). (d) Binding
properties of hemocytes of larval Orgyia following parasitism by Cotesia (after Guzo & Stoltz, 1987).
that the nodulation response is modulated by eicosanoids complete within 24 hours. The cells adjacent to the object
(Miller et al., 1996). become necrotic. Melanin is often produced in this layer as
a consequence of the activation of the prophenoloxidase
Encapsulation Larger invaders, such as parasitoid larvae system. Cells in the adjacent layers become flattened and
or nematodes, evoke a third type of response. They are intercellular junctions, primarily tight junctions and
encapsulated by large numbers of hemocytes. desmosomes, develop between them. On the outside the
Granulocytes discharge their contents at the surface of the cells are less modified.
invader. This can occur within five minutes of the inva- Encapsulation normally occurs if the parasite is in an
sion. After about 30 minutes, plasmatocytes are attracted unusual host although the means by which it is killed are
and start to accumulate. More plasmatocytes adhere to the not understood.
outside of the clump so that the object becomes sur-
rounded by a capsule comprising several layers of cells. 5.3.3 Humoral responses
The number of cell layers varies with the species and the Damage to the epidermis, even without infection, induces
physical and chemical nature of the surface of the object some increase in the amounts of hemolymph proteins, but
encapsulated. Recruitment of new hemocytes is usually the effect is greatly enhanced by bacterial infection even if
IMMUNITY 125
Fig. 5.33. Nodule formation (after Ratcliffe & Gagen, 1977). (a) One minute after injection of bacteria. Granulocytes have
degranulated and bacteria are trapped in the flocculent material produced by the cells. (b) Thirty minutes after injection. The
clumps of granulocytes and bacteria have compacted, and melanization of the matrix is beginning. (c) Plasmatocytes arrive at
the nodule and melanization of the matrix is advanced. (d) Twenty-four hours after injection. Nodulation is complete. Three
regions are recognizable in the layers of plasmatocytes.
the bacteria are dead. There is evidence that the response amino acids (20 kDa). They are synthesized mainly in the
is elicited by peptidoglycans from the cell walls of the bac- fat body, but also by some hemocytes and the quantity of
teria. cecropins produced increases with the number of bacteria
The hemolymph of the pupa of Hyalophora normally injected into the hemolymph. These proteins are bacteri-
contains a small protein (48 kDa) known as hemolin. In cidal, different proteins in each class exhibiting different
Manduca, its synthesis is induced by bacterial infection. It specificities in their effectiveness against different species
is a member of the immunoglobulin family of proteins that of bacteria. The induction of the different proteins is,
are important in the immune systems of vertebrates. however, the same irrespective of the nature of the bacter-
Peptidoglycans produce an increase in the amount of ial infection. Comparable proteins, often belonging to
hemolin present and this appears to initiate the synthesis different protein families, have been found in a number of
of a suite of proteins: a total of 15 different proteins in other insects (For example, Chernysh et al., 1996).
Hyalophora and 25 in Manduca larvae. These include two In addition to these proteins, lysozymes are also
major families of proteins known as the cecropins and the induced by infection. These enzymes have been found in a
attacins. The cecropins are peptides of 35–37 amino acids variety of insects, including Locusta and the house cricket,
(4 kDa), the attacins are bigger, consisting of chains of 188 Gryllus. They appear to complement the action of
126 CIRCULATORY SYSTEM, BLOOD AND IMMUNE SYSTEMS
cecropins and cecropin-like proteins by digesting the bac- (Guzo & Stoltz, 1987). Clearly, the caterpillar is deprived
terial cell walls remaining after attack by other proteins. of its ability to encapsulate the parasite. In the larva of the
Amongst the Diptera, a process analogous to turnip moth, Agrotis, activation of the prophenoloxidase in
encapsulation occurs, but apparently without the involve- the hemolymph is suppressed both by a parasitic nematode
ment of hemocytes. This process is known as humoral and by the nematode’s symbiotic bacteria (Yokoo, Tojo &
encapsulation. It is only known to occur in Chironomidae Ishibashi, 1992).
and other small Diptera with cell counts of less than 6000 The processes involved in suppressing the host’s
hemocytes l⫺1. Perhaps normal cellular mechanisms are response are best understood in parasitic Hymenoptera of
inefficient when the cell count is so low. Some 2–15 the families Braconidae and Ichneumonidae. Some of
minutes after a foreign particle enters the hemolymph, these insects, such as Cotesia, carry a virus in the calyces of
strands of material begin to accumulate round it. More the ovaries. The virus, of a type called a polydna virus, is
material is added until the invader is completely enclosed probably species-specific and it replicates in cells of the
in a capsule one or more microns thick. The capsule calyx from which it is released into the lumen of the
becomes melanized, but some descriptions suggest that oviduct. When the wasp oviposits in a host, she also injects
the protein of the capsule may become altered in some way a venom which probably serves to immobilize the prey,
analogous to cuticular sclerotization. Tyrosine from the proteins secreted by the ovary, and the virus. Although it
hemolymph is utilized during the process. Humoral does not replicate in the host, the virus invades the host
encapsulation appears to be a highly efficient means of iso- tissues and causes them to produce novel proteins. Its
lating potential pathogens, and the larvae of Chironomus effectiveness may be synergized by components of the
are able to withstand the injection of relatively high doses venom. In larval Manduca parasitized by the braconid
of highly pathogenic bacteria. Bacteria, fungi and nema- Cotesia, some new proteins appear even before the para-
todes can all be encapsulated by this mechanism. sitoid hatches and within 24 hours of oviposition they may
Reviews: Boman & Hultmark, 1987; Götz & Vey, 1986 – humoral constitute 10% of the protein in the host hemolymph. It is
encapsulation suggested that they bind to the surface of the newly
hatched parasitoid larva and inhibit the encapsulation by
5.3.4 Overcoming the immune response the host hemocytes.
In the habitual host of a pathogen, or parasite, the invading In addition to suppressing the host’s immune response,
organism usually survives. It is enabled to do this by over- some parasitoids modify the development of their hosts. A
coming, or by modifying, the host’s normal response. caterpillar of Pseudaletia parasitized by the wasp Cotesia
Organisms that normally are encapsulated may avoid produces a growth-blocking peptide, probably in response
encapsulation, or break free of the capsule. For example, to the virus injected by the wasp. This peptide reduces the
as the germinating hyphae of the fungus Metarhizium production of juvenile hormone esterase and, it is
penetrate the cuticle of Schistocerca, the host’s hemocytes believed, in this way a high titer of juvenile hormone is
aggregate beneath the point of entry. The fungal wall maintained in the host hemolymph. This delays meta-
contains –1,3-glucans which presumably initiate the morphosis of the host. This is thought to be important
defensive response, but this response is suppressed by because the wasp would be unable to escape from the
compounds consisting of five cyclically linked amino heavily sclerotized pupa (Hayakawa, 1995).
acids, known as destruxins, produced by the fungus Reviews: Beckage et al., 1993; Lavine & Beckage, 1995
(Huxham, Lackie & McCorkindale, 1989).
The larva of the braconid parasite, Cotesia, perma-
5.4 CONNECTIVE TISSUE
nently suppresses encapsulation by the hemocytes of the
larval tussock moth, Orgyia. After an initial period of Insect connective tissue contains collagen fibers, and
elevation, the hemocyte count declines below the normal sometimes also elastin, glycosaminoglycans and glycopro-
level and remains low. A similar response is produced by teins. Collagen is a protein made up of three polypeptide
injecting the venom and the calyx fluid of the female para- chains with a helical structure. Glycine accounts for about
sitoid (Fig. 5.32c). The tendency of plasmatocytes to 33% of the total amino acids and proline another 20%.
adhere to surfaces is also greatly reduced (Fig. 5.32d) The molecular spacing in fibrous collagen is very precise,
REFERENCES 127
giving rise to a characteristic banded appearance. tures, giving the layer an almost cellular appearance. The
Glycosaminoglycans are long chain polymers formed from significance of this structure is not known.
disaccharide units. Each disaccharide consists of an amino Connective tissue is produced by the cells which it
sugar and another sugar or related molecule. underlies and by fibroblasts within the matrix. Hemocytes
Glycosaminoglycans are large molecules which form a also contribute to the basal lamina surrounding the hemo-
major component of the connective tissue. Many different coel (Sass, Kiss & Locke, 1994). In holometabolous insects,
glycoproteins are present. larval connective tissues are largely destroyed during the
A fibrous connective tissue layer, usually 1 to 10 m pupal period and replaced by newly formed material. These
thick, surrounds many organs and may form a matrix new structures are not produced until the underlying tissues
within tissues, between muscle fibers, for example. It also are complete and they are absent from dividing tissues.
forms a layer, the neural lamella, around the whole of the The usual functions of connective tissue are those of
central nervous system (section 20.1.2). A thick layer, supporting and binding tissues together, although in
about 80 m thick, surrounds the ejaculatory duct of male insects the tracheal system also functions in this way to
Locusta. A basal lamina, or basement membrane, is present some extent. It is also possible that the elastic properties of
beneath epithelia and surrounds fat body and muscles. It some connective tissues are important. For example, the
comprises an electron-lucent layer and an outer dense elasticity of the tunica propria (section 13.3) may help to
layer, but as fibrous connective tissue is produced beneath squeeze oocytes from the ovarioles into the oviduct. It has
it the electron lucent layer may disappear. The basal also been suggested that the thickening of the epidermal
lamina of the midgut is complex in some beetles and bugs basal lamina which occurs just before apolysis in Rhodnius
and in the mosquito, Aedes. In the larva of Oryctes, for enables it to serve as a base for the forces used in molding
example, it is three layered and each layer is composed of the new cuticle.
electron dense units surrounding larger, less dense struc- Review: Ashhurst, 1985
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267–73. New York: Liss. Insects. In Invertebrate Blood Cells vol. between haemolymph transport and
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of insects: an ultrastructural analysis of 407–21. flows in the wings of pierid butterflies
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Tissue & Cell, 9, 73–85. (1988). Lipid transport in insects. Lepidoptera). Zoomorphology, 103,
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ed. A.P. Gupta, pp. 331–414. populations. In Insect Hemocytes, ed. Morphology, 63, 229–61.
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Ratcliffe, N.A. & Walters, J.B. (1983). Strand, M.R. & Pech, L.L. (1995). development and colony founding.
Studies on the in vivo cellular reactions Immunological basis for compatibility Journal of Insect Physiology, 41, 885–94.
of insects: clearance of pathogenic and in parasitoid-host relationships. Annual Wiesner, A., Wittwer, D. & Götz, P.
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mellonella larvae. Journal of Insect Sutcliffe, D.W. (1963). The chemical ing factor is released by and acts on
Physiology, 29, 407–15. composition of haemolymph in insects phagocytosing Galleria mellonella
and some other arthropods, in relation haemocytes in vitro. Journal of Insect
to their phylogeny. Comparative Physiology, 42, 829–35.
Biochemistry and Physiology, 9, 121–35.
REFERENCES 131
Wigglesworth, V.B. (1972). The Principles Yokoo, S., Tojo, S. & Ishibashi, N. (1992). Ziegler, R., Willingham, L.A., Sanders,
of Insect Physiology. London: Chapman Suppression of the prophenoloxidase S.J., Tamen-Smith, L. & Tsuchida, K.
& Hall. cascade in the larval haemolymph of (1995). Apolipophorin-III and adipoki-
the turnip moth, Agrotis segetum by an netic hormone in lipid metabolism of
entomopathogenic nematode, larval Manduca sexta. Insect
Steinernema carpocapsae and its symbi- Biochemistry and Molecular Biology, 25,
otic bacterium. Journal of Insect 101–8.
Physiology, 38, 915–24.
6 Fat body
[132]
STRUCTURE 133
c)
0.1 m
b) 1.0 m
gap junction
a)
mitochondria
basal lamina
lipid
droplet
plasma membrane
reticular system
desmosome
rough
endoplasmic
reticulum
d)
0.1 m
Fig. 6.2. Structure of a mature trophocyte. (a) Diagram of a trophocyte. (b) Transmission electron micrograph of the plasma
membrane reticular system of a trophocyte from the larva of Calpodes. (c) Gap junction between two trophocytes in the fat
body of Calpodes. (d) Desmosome joining two trophocytes in the fat body of Calpodes (b, c and d after Dean et al., 1985).
134 FAT BODY
a) frequency of mitoses
charged and the effect of this is to limit the access of some
large charged molecules to the interior of the reticulum. It
ecdysis ecdysis
larva 4 larva 5
is possible that the reticulum is concerned with the recep-
pupa
prep synthetic
tion and unloading of lipophorins (Locke, 1986; Locke &
phase phase Huie, 1983). When the larva is approaching the molt to
frequency
protein for the blue-colored protein is formed de novo at the stimulated by juvenile hormone, although in Diptera this
time of pupation. This receptor is only present in the mem- function is performed by ecdysteroids (see Fig. 13.10).
branes of cells in the perivisceral fat body, not in the Juvenile hormone perhaps inhibits the synthesis of dia-
peripheral fat body (Wang & Haunerland, 1993). Although pause proteins in Leptinotarsa, but the differences in the
some increase in cell size occurs as lipid and glycogen accu- timing of production of the different proteins suggests
mulate, the uptake of proteins is associated with a consider- that the regulation is complex (Dortland, 1978). Protein
able increase in the volumes of the fat body cells (Fig. 6.5). uptake into the fat body has been shown to be initiated by
While in general it appears that synthesis and storage 20-hydroxyecdysone in a number of insects. Perhaps the
of proteins do not occur simultaneously, in prediapause hormone acts via its regulation of receptor proteins in the
adults of Leptinotarsa, two diapause proteins are stored cell membranes of the trophocytes.
while synthesis continues. Tyrosine is a key chemical in cuticle sclerotization and
The factors regulating protein synthesis and storage insects accumulate it before a molt (section 16.5.3). In
are not known with certainty although both juvenile some insects, it is taken up from the hemolymph and
hormone and ecdysteroids may be involved. Juvenile stored in large vacuoles in the trophocytes. This has been
hormone suppresses synthesis of arylphorin in the silk- most comprehensively studied in the fourth stage larva of
worm, Bombyx. Synthesis starts in the final larval stage Calpodes where the uptake of tyrosine begins about one
when juvenile hormone disappears from the hemolymph day after ecdysis. Shortly before the next ecdysis, tyrosine
(Tojo, Kiguchi & Kimura, 1981). On the other hand, in is released into the hemolymph (Fig. 6.6). Accumulation in
adult insects of most orders, synthesis of vitellogenin is the fat body, which is an alternative to storing tyrosine as a
FUNCTIONS 137
concentration (mg.ml-1 )
The fat body is also a major site of transamination 16
starved
between amino acids (section 4.1.1). fed
14
6.2.2 Carbohydrates 12
Carbohydrate is stored as glycogen which, in caterpillars,
10
and probably also in other insects, is built up in the fat
body during periods of active feeding. This store becomes
depleted during sustained activity or over a molt, when the b) glucose
a) b)
20 15
amount (µg.mg -1)
absorbed phospholipid
15
weight (mg)
10
growth
10
5
5
triacylglyceride
0 0
1 2 3 4 5 6 7 0 2 4 6 8
age (days) glucose (%)
c)
50
40
amount (%)
30
20 0% glucose
10 6% glucose
0
16:0 16:1 18:0 18:1
compound
Fig. 6.9. Lipogenesis from carbohydrate. (a) The daily amount of lipid absorbed and the daily increase in lipid content during
the last stage larva of Locusta. The increase in lipid in the first three days greatly exceeds the intake of lipid, implying that
FUNCTIONS 139
but may also occur in the ovaries and other tissues. It added to the acyl group at each of the final steps, the fatty
involves the synthesis of fatty acids, frequently followed by acids produced generally have an even number of carbon
their incorporation into triacylglycerol. The primary atoms. In most insect species so far studied, the most com-
building block for fatty acids is the acetyl group monly produced primary product of fatty acid synthesis is
(CH3.CO⫺). In insects, this is known to be derived from palmitic acid (16 carbon atoms), but myristic acid (C14) is
acetate, glucose, or the amino acid, leucine. Combined produced by some flies and aphids, while stearic acid (C18)
with coenzyme A, which acts as a carrier, the active acetyl is the initial product in a hymenopteran parasitoid.
group is carboxylated to form malonyl-coenzyme A. The Following this, further elongation and desaturation may
malonyl group contains three carbon atoms and by further occur to produce the fatty acids required by the insects (see
condensation reactions with acetyl-coenzyme A and then Fig. 4.3). A large proportion of the fatty acids produced, as
with malonyl-coenzyme A, fatty acids of increasing chain well as those derived directly from the diet, are sub-
length are produced (Fig. 6.10). As two carbon atoms are sequently combined to form triacylglycerol.
It is not known if there is any factor stimulating lipid its release is regulated. Low levels of trehalose in the
synthesis, but there is considerable evidence that juvenile hemolymph produced early in the flight of the locust may
hormone inhibits synthesis. The mechanism of action, stimulate release of adipokinetic hormone, but probably
however, is not known. The mobilization of lipids from do not initiate it. Information from the brain is trans-
the fat body is known to be effected by the neuro- mitted via the nerves connecting it with the corpora car-
hormone, octopamine, and by adipokinetic hormone. diaca and this results in release of the hormone. Both
Octopamine appears in the hemolymph when an insect is octopamine and adipokinetic hormone interact with
disturbed. In the desert locust, Schistocerca, it’s titer receptor sites on the plasma membrane of fat body cells
increases fourfold within ten minutes of the start of flight and elevate the production of cAMP. This activates a
while the hemolymph titer of adipokinetic hormone protein kinase which, in turn, activates a triacylglycerol
reaches a maximum after about 30 minutes of flight, and kinase catalyzing the conversion of triacylglycerol to dia-
then is sustained at a lower level for some time. cylglycerol (Fig. 6.11). Lipophorin then transports the
Adipokinetic hormone is released from the corpora car- diacylglycerol in the hemolymph (section 5.2.2.3).
diaca during flight in many insects. It is not certain how Reviews: Downer, 1985; Steele, 1985; Wheeler, 1989
REFERENCES 141
REFERENCES
Bergtrom, G., Gittelman, S., Laufer, H. & Keeley, L.L. (1985). Physiology and bio- Simpson, S.J. (1982). Changes in the
Ovitt, C. (1976). Haemoglobin syn- chemistry of the fat body. In efficiency of utilisation of food
thesis in Bueonoa confusa (Hemiptera). Comprehensive Insect Physiology, throughout the fifth-instar nymphs of
Insect Biochemistry, 6, 595–600. Biochemistry and Pharmacology, vol. 3, Locusta migratoria. Entomologia
Butterworth, F.M., Bodenstein, D. & ed. G.A. Kerkut & L.I. Gilbert, pp. Experimentalis et Applicata, 31, 265–75.
King, R.C. (1965). Adipose tissue of 211–48. Oxford: Pergamon Press. Steele, J.E. (1985). Control of metabolic
Drosophila melanogaster I. An experi- Locke, M. (1970). The molt/intermolt processes. In Comprehensive Insect
mental study of larval fat body. cycle in the epidermis and other tissues Physiology, Biochemistry and
Journal of Experimental Zoology, 158, of an insect Calpodes ethlius Pharmacology, vol. 8, ed. G.A. Kerkut
141–54. (Lepidoptera, Hesperiidae). Tissue & & L.I. Gilbert, pp. 99–145. Oxford:
Dean, R.L., Locke, M. & Collins, J.V. Cell, 2, 197–223. Pergamon Press.
(1985). Structure of the fat body. In Locke, M. (1984). The structure and Thompson, S.N. (1979a). Effect of dietary
Comprehensive Insect Physiology, development of the vacuolar system in glucose on in vitro fatty acid metabo-
Biochemistry and Pharmacology, vol. 3, the fat body of insects. In Insect lism and in vitro synthetase activity in
ed. G.A. Kerkut & L.I. Gilbert, pp. Ultrastructure, vol. 2, ed. R.C. King & the insect parasite, Exeristes roborator
155–210. Oxford: Pergamon Press. H. Akai, pp. 151–97. New York: (Fabricius). Insect Biochemistry, 9,
Dortland, J.F. (1978). Synthesis of vitel- Plenum Press. 645–51.
logenins and diapause proteins by the Locke, M. (1986). The development of Thompson, S.N. (1979b). The effects of
fat body of Leptinotarsa, as a function of the plasma membrane reticular system dietary carbohydrate on larval develop-
photoperiod. Physiological Entomology, in the fat body of an insect. Tissue & ment and lipogenesis in the parasite,
3, 281–8. Cell, 18, 853–67. Exeristes roborator (Fabricius)
Downer, R.G.H. (1985). Lipid metabo- Locke, M. & Huie, P. (1983). A function (Hymenoptera: Ichneumonidae).
lism. In Comprehensive Insect for plasma membrane reticular systems. Journal of Parasitology, 65,
Physiology, Biochemistry and Tissue & Cell, 15, 885–902. 849–54.
Pharmacology, vol. 10, ed. G.A. Kerkut Martoja, R. (1976). Le corps gras ou tissu Tojo, S., Kiguchi, K. & Kimura, S. (1981).
& L.I. Gilbert, pp. 77–113. Oxford: adipeux. In Traité de Zoologie, vol. 8, Hormonal control of storage protein
Pergamon Press. part 4, ed. P.-P.Grassé, pp. 407–90. synthesis and uptake by the fat body in
Friedman, S. (1985). Carbohydrate Paris: Masson et Cie. the silkworm, Bombyx mori. Journal of
metabolism. In Comprehensive Insect McDermid, H. & Locke, M. (1983). Insect Physiology, 27, 491–7.
Physiology, Biochemistry and Tyrosine storage vacuoles in insect fat Ueno, K. & Natori, S. (1984).
Pharmacology, vol. 10, ed. G.A. Kerkut body. Tissue & Cell, 15, 137–58. Identification of storage protein recep-
& L.I. Gilbert, pp. 43–76. Oxford: Miller, P.L. (1966). The function of tor and its precursor in the fat body
Pergamon Press. haemoglobin in relation to the mainte- membrane of Sarcophaga peregrina.
Gies, A., Fromm, T. & Ziegler, R. (1988). nance of neutral buoyancy in Anisops Journal of Biological Chemistry, 259,
Energy metabolism in starving larvae of pellucens (Notonectidae, Hemiptera). 12107–11.
Manduca sexta. Comparative Biochemistry Journal of Experimental Biology, 44, Wang, Z. & Haunerland, N.H. (1993).
and Physiology, 91A, 549–55. 529–43. Storage protein uptake in Helicoverpa
Haunerland, N.H., Nair, K.N. & Bowers, Palli, S.R. & Locke, M. (1988). The syn- zea. Journal of Biological Chemistry,
W.S. (1990). Fat body heterogeneity thesis of hemolymph proteins by the 268, 16673–8.
during development of Heliothis zea. larval fat body of an insect Calpodes Wheeler, C.H. (1989). Mobilization and
Insect Biochemistry, 20, 829–37. ethlius (Lepidoptera: Hesperiidae). transport of fuels to the flight muscles.
Haunerland, N.H. & Shirk, P.D. (1995). Insect Biochemistry, 18, 405–13. In Insect Flight, ed. G.J. Goldsworthy &
Regional and functional differentiation Schin, K., Laufer, H. & Carr, E. (1977). C.H. Wheeler, pp. 273–303. Boca
in the insect fat body. Annual Review of Cytochemical and electrophoretic Raton: CRC Press.
Entomology, 40, 121–45. studies of haemoglobin synthesis in the
fat body of a midge, Chironomus
thummi. Journal of Insect Physiology,
23, 1233–42.
PART II
The skeleton of the thoracic segments is modified to give inflected. The narrow rim in front of the sulcus is called the
efficient support for the legs and wings, and the musculature acrotergite (Figs. 7.1b, 7.2). An acrotergite never occurs at
is adapted to produce the movements of these appendages. the front of the prothorax because the anterior part of this
segment forms part of the neck and the muscles from the
head pass directly to the acrotergite of the mesothorax.
7.1 SEGMENTATION
An area at the back of each segment remains membra-
In larval holometabolous insects the cuticle is soft and nous, forming a new intersegmental membrane. This
flexible, or only partially sclerotized, and the longitudinal does not correspond with the original intersegmental
muscles are attached to the intersegmental folds (Fig. 7.1a). groove and so a secondary segmentation is superimposed
This represents a primitive condition comparable with that on the first, but neither corresponds precisely with the
occurring in the annelids. Insects with this arrangement ‘parasegments’ defined by molecular studies (see section
move as a result of successive changes in the shapes of the 14.2.5).
thoracic and abdominal segments (section 8.4.3), these This basic condition with a membranous area at the
changes of shape being permitted by the flexible cuticle. posterior end of each segment occurs in the abdomen
When the cuticle is sclerotized, sclerites in the interseg- where this is sclerotized, in the meso- and meta-thoracic
mental folds which have the longitudinal muscles attached segments of larval insects with a sclerotized thorax, in the
to them are usually fused with the segmental sclerites Apterygota and in adult Blattodea and Isoptera where the
behind. The large sclerite on the dorsal surface of a segment wings are not moved by indirect muscles. With this
is called the tergum, or, in the thorax, the notum. Anteriorly arrangement, contraction of the longitudinal muscles pro-
it incorporates the intersegmental region, the original fold duces telescoping of the segments.
being marked by the antecostal sulcus where the cuticle is Review: Zrzavy & Stys, 1995
a) unsclerotized first
larva abdominal
prothorax mesothorax metathorax segment
longitudinal
muscle
intersegmental antecostal
notum acrotergite
b) apterygote membrane sulcus
antecostal
ridge
c) winged postnotum
adult
phragma longitudinal
flight muscle
Fig. 7.1. Segmentation and the derivation of the postnotum and phragmata in pterygote insects. Sclerotized areas are
indicated by a solid line, membranous areas by a double line.
146 THORAX
acrotergite antecostal
7.2 THORAX sulcus
transverse
prescutum sulcus
The thorax consists of three segments known as the pro-, prealar arm
meso- and meta-thoracic segments. In most insects all
anterior notal
three segments bear a pair of legs, but this is not the case in scutum process
larval Diptera, larval Hymenoptera Apocrita, some larval
scutoscutellar
Coleoptera and a small number of adult insects which are sulcus
apodous. In addition, winged insects have a pair of wings
posterior notal
on the meso- and meta-thoracic segments and these two process
scutellum
segments are then collectively known as the pterothorax. axillary cord
Reviews: Matsuda, 1970, 1979; Snodgrass, 1935
Fig. 7.2. Notum of a wing-bearing segment. Stippled areas are
membrane at base of wing (axillary sclerites not shown). Names
7.2.1 Morphology of the thorax
of sclerites in italics (after Snodgrass, 1935).
Tergum The tergum of the prothoracic segment is known
as the pronotum. It is often small serving primarily for
attachment of the muscles of the first pair of legs, but in into areas. Often a transverse sulcus divides the notum into
Orthoptera, Blattodea and Coleoptera it forms a large plate an anterior prescutum and a scutum, while a V-shaped
affording some protection to the pterothoracic segments. sulcus posteriorly cuts off the scutellum (Fig. 7.2). These
The meso- and meta-nota are relatively small in wingless areas are commonly demarcated, but, because of their
insects and larvae, but in winged insects they become origins as functional units, plates of the same name in
modified for the attachment of the wings. In the majority of different insects are not necessarily homologous. In addition,
winged insects the downward movement of the wings the lateral regions of the scutum may be cut off by a sulcus or
depends on an upwards distortion of the dorsal wall of the there may be a median longitudinal sulcus. Commonly, the
thorax (section 9.7.1). This is made possible by a prescutum connects with the pleuron by an extension, the
modification of the basic segmental arrangement. The prealar arm, in front of the wing, while behind the wing a
acrotergites of the metathorax and the first abdominal postalar arm connects the postnotum to the epimeron (Fig.
segment extend forwards to join the tergum of the segment 7.5b). Laterally the scutum is produced into two processes,
in front and in many cases become secondarily separated the anterior and posterior notal processes, which articulate
from their original segment by a narrow membranous with the axillary sclerites in the wing base (see Fig. 9.13).
region. Each acrotergite and antecostal sulcus is now known The posterior fold of the scutellum continues as the axillary
as a postnotum (Fig. 7.1c). There may thus be a mesopost- cord along the trailing edge of the wing.
notum and a metapostnotum if both pairs of wings are more
or less equally important in flight, but where the hind wings Sternum The primary sclerotizations on the ventral side
provide most power, as in Orthoptera and Coleoptera, only are segmental and inter segmental plates which often
the metapostnotum is developed. The Diptera on the other remain separate in the thorax. The intersegmental sclerite
hand, using only the forewings for flight, have a well devel- is produced internally into a spine and is called the
oped mesopostnotum, but no metapostnotum. To provide spinasternum, while the segmental sclerite is called the
attachment for the large longitudinal muscles moving the eusternum (Fig. 7.6). Various degrees of fusion occur so
wings, the antecostal ridges at the front and back of the that four basic arrangements may be found:
mesothorax and the back of the metathorax usually develop
into extensive internal plates, the phragmata (Figs. 7.1c and a) all elements separate – eusternum of prothorax; first
7.6). Which of the phragmata are developed depends again spina; eusternum of mesothorax; second spina; euster-
on which wings are most important in flight. num of metathorax (see Fig. 7.3a. Notice that in the
Various strengthening ridges develop on the tergum of a diagram eusternum is divided into basisternum and
wing-bearing segment. These are local adaptations to the sternellum);
mechanical stresses imposed by the wings and their muscles. b) eusternum of mesothorax and second spina fuse, the
The ridges appear externally as sulci which divide the notum rest remaining separate;
THORAX 147
basisternum
metathorax
sternellum
sternal
apophysis
first abdominal
sternum
b) Nomadacris
sternal
apophysis basisternum
base of sternellum prothorax
coxa 1
spinasternum
spina
presternum
basisternum
mesothorax
sternal
apophysis
sternellum
coxa 2
spina basisternum
metathorax
sternal
apophysis sternellum
first abdominal
coxa 3 sternum
148 THORAX
presternum spinasternum
basisternum sternellum
mesonotum dorsal longitudinal oblique dorsal Fig. 7.6. The main muscles, other
muscle muscle than the leg muscles, in the
pronotum
postnotum mesothorax of a winged insect (after
Snodgrass, 1935).
phragma
wing flexor
muscle
pleural
apohysis oblique intersegmental
muscle
coxa sternopleural
muscle
spina
eusternum
spina sternal
eusternum apophysis spinasternum
relatively poorly developed in sclerotized larvae, in adult sternal apophysis to the next in adult insects, producing
Odonata, Blattodea and Isoptera which have direct wing some ventral telescoping of the thoracic segments.
depressor muscles, and also in secondarily wingless groups Dorso-ventral muscles run from the tergum to the
such as Siphonaptera. In these cases they tend to telescope pleuron or sternum. They are primitively concerned with
one segment into the next, while the more lateral muscles rotation or compression of the segment, but in winged
rotate the segments relative to each other. In unsclerotized insects they are important flight muscles (section 9.7.1). In
insects, contraction of the longitudinal muscles shortens larval insects an oblique intersegmental muscle runs from
the segment. the sternal apophysis to the anterior edge of the following
In most winged insects, however, the dorsal longitudi- tergum or pleuron, but in adults it is usually only present
nal muscles are the main wing depressors and they are well between prothorax and mesothorax.
developed (section 9.7.1; Fig. 7.6), running from phragma The other important muscles of the thorax are con-
to phragma so that their contraction distorts the segments. cerned with movement of the legs and wings. They are
The ventral longitudinal muscles run mainly from one dealt with separately (sections 8.1.1, 9.6).
150 THORAX
REFERENCES
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8 Legs and locomotion
Insects typically have three pairs of legs, one pair on each The femur is often small in larval insects, but in most
of the thoracic segments. From this, the alternative name adults it is the largest and stoutest part of the leg. It is
for insects, the ‘hexapods’, is derived, although not all often more or less fixed to the trochanter and moves with
hexapods are now regarded as insects. it. In this case, there are no muscles moving the femur
with respect to the trochanter, but sometimes a single
muscle arising in the trochanter is able to produce a slight
8.1 BASIC STRUCTURE OF THE LEGS
backward movement, or reduction, of the femur (Fig.
Each leg consists typically of six segments, articulating 8.5b).
with each other by mono- or di-condylic articulations set in The tibia is the long shank of the leg articulating with
a membrane, the corium. The six basic segments are coxa, the femur by a dicondylic joint so that it moves in a vertical
trochanter, femur, tibia, tarsus and pretarsus (Fig. 8.1a). plane (Fig. 8.1c,d). In most insects, the head of the tibia is
The coxa is often in the form of a truncated cone and bent so that the shank can flex right back against the femur
articulates basally with the wall of the thorax. There may (Fig. 8.1a). The tarsus, in most insects, is subdivided into
be only a single articulation with the pleuron (Fig. 8.2a), in from two to five tarsomeres. These are differentiated from
which case movement of the coxa is very free, but fre- true segments by the absence of muscles. The basal tar-
quently there is a second articulation with the trochantin somere, or basitarsus, articulates with the distal end of the
(Fig. 8.2b). This restricts movement to some extent, but, tibia by a single condyle (Fig. 8.1e), but between the tar-
because the trochantin is flexibly joined to the episternum, someres there is no articulation; they are connected by
the coxa is still relatively mobile. In some higher forms flexible membrane so that they are freely movable. In
there are rigid pleural and sternal articulations limiting Protura, some Collembola and the larvae of most
movement of the coxa to rotation about these two points holometabolous insects, the tarsus is unsegmented (Fig.
(Fig. 8.2c). In the Lepidoptera the coxae of the middle and 8.4c) or, in the latter, may be fused with the tibia.
hind legs are fused with the thorax and this is also true of The pretarsus, in the majority of insects, consists of a
the hind coxae in Adephaga. membranous base supporting a median lobe, the arolium,
The part of the coxa bearing the articulations is often which may be membranous or partly sclerotized, and a
strengthened by a ridge indicated externally by the basi- pair of claws which articulate with a median process of the
costal sulcus which marks off the basal part of the coxa as last tarsomere known as the unguifer. Ventrally there is a
the basicoxite (Fig. 8.3a). The basicoxite is divided into basal sclerotized plate, the unguitractor, and between this
anterior and posterior parts by a ridge strengthening the and the claws are small plates called auxiliae (Fig. 8.4a). In
articulation, the posterior part being called the meron. Diptera, a membranous pulvillus arises from the base of
This is very large in Neuroptera, Mecoptera, Trichoptera each auxilia while a median empodium, which may be
and Lepidoptera (Fig. 8.3b), while in the higher Diptera it spine- or lobe-like, arises from the unguitractor (Fig.
becomes separated from the coxa altogether and forms a 8.4b). There is no arolium in Diptera other than
part of the wall of the thorax. Tipulidae. The development of the claws varies in
The trochanter is a small segment with a dicondylic different insect groups. Commonly they are more or less
articulation with the coxa such that it can only move in the equally well-developed, but in Thysanoptera they are
vertical plane (Fig. 8.1b). In Odonata there are two minute and the pretarsus consists largely of the bladder-
trochanters and this also appears to be the case in like arolium. In other groups, the claws develop
Hymenoptera, but here the apparent second trochanter is, unequally; one may fail to develop altogether, so that in
in fact, a part of the femur. Ischnocera, for instance, there is only a single claw. In
[151]
152 LEGS AND LOCOMOTION
a)
femur
flexor
muscle
coxa
proximal end
tibia of tibia
trochanter
d)
tarsus
distal end
of femur
pretarsus
proximal end
of tibia
apodemes of
levator muscles
b)
Fig. 8.1. Leg and articulations. Points of articulation shown by bold arrows (mainly after Snodgrass, 1935, 1952). (a) Typical
insect leg. (b) Dicondylic articulation of trochanter with coxa and the apodemes of muscles moving the trochanter. Notice
that the femur is united with the trochanter; there is no moving joint. (c), (d) dicondylic articulation of tibia and femur, (c)
side view, (d) end view. (e) Monocondylic, ball articulation of tarsus with tibia.
Protura, some Collembola and many holometabolous thorax and a fairly typical arrangement is shown in Fig.
larvae the entire pretarsus consists of a single claw-like 8.5a with promotor and remotor muscles arising on the
segment (Fig. 8.4c). tergum, abductor and adductor muscles from the pleuron
and sternum, and rotator muscles also from the sternum
8.1.1 Muscles of the legs (see section 8.4.1.1. for definitions). The roles of the
The muscles which move the legs fall into two categories: muscles vary, depending on the activities of other muscles
extrinsic, arising outside the leg, and intrinsic, wholly and also on the type of articulation. In Apis
within the leg and running from one segment to another. (Hymenoptera), which has rigid pleural and sternal
The coxa is moved by extrinsic muscles arising in the articulations, promotor and remotor muscles from the
BASIC STRUCTURE OF THE LEGS 153
a) b) c)
anterior
episternum
epimeron
pleural pleural sulcus
articulation
flexible pleural
connection articulation
trochantin
coxa trochantinal
articulation
sternal
sternum articulation
Fig. 8.2. Three types of coxal articulation with the thorax. Points of articulation shown by arrows. Membranous regions
stippled (after Snodgrass, 1935).
basicoxite
meron
basicostal
sulcus
coxal
sulcus membrane
articulations with
trochanter
pulvillus
auxilia
auxilia
unguitractor unguitractor tibia
tarsal depressor
distal muscle
tarsomere distal
tarsomere
spur tarsus
apodeme for attachment
of pretarsal depressor
muscle
pretarsus
Fig. 8.4. Pretarsus. (a) Pretarsus of Periplaneta, ventral view (after Snodgrass, 1935). (b) Pretarsus of a dipteran, ventral view
(after Snodgrass, 1935). (c) Distal part of prothoracic leg of larval Triaenodes (Trichoptera) showing a simple pretarsal
segment (after Tindall, 1964).
154 LEGS AND LOCOMOTION
trochanter
depressor
muscles pretarsal
depressor
muscles
tibial
flexor
muscles tarsal
femoral levator
reductor muscle
muscle
tarsal pretarsal
depresssor apodeme
muscle
tergum are absent. In the pterothoracic segments, muscles trochanter, but the tibia is moved by extensor and flexor
(insertions marked with oblique hatching in Fig. 8.5a) run muscles arising in the femur and inserted into apodemes
from the coxae to the basalar and subalar sclerites. They from the membrane at the base of the tibia (see Fig. 8.21a).
are concerned with movements of the wings as well as the Levator and depressor muscles of the tarsus arise in the
legs. tibia and are inserted into the proximal end of the basitar-
The intrinsic musculature is much simpler than the sus, but there are no muscles within the tarsus moving the
coxal musculature, consisting typically only of pairs of tarsomeres.
antagonistic muscles in each segment (Fig. 8.5b). In It is characteristic of the insects that the pretarsus has a
Periplaneta, there are three levator muscles of the depressor muscle, but no levator muscle. The fibers of the
trochanter arising in the coxa and three depressor muscles, depressor occur in small groups in the femur and tibia and
two again with origins in the coxa and a third arising on the are inserted into a long apodeme which arises on the
pleural ridge and the tergum. unguitractor (Figs. 8.5b, 8.21a). Levation of the pretarsus
The femur is usually immovably attached to the results from the elasticity of its basal parts.
BASIC STRUCTURE OF THE LEGS 155
8.1.3 Adhesion
Many insects are able to climb and hold on to smooth sur-
faces. Different insects use different structures and proba-
bly different mechanisms for adhesion, but many use
adhesive setae, also sometimes called tenent hairs. These
setae are grouped together to form adhesive pads which
occur on various parts of the legs. Rhodnius and some other
Reduviidae have adhesive pads at the distal ends of the
tibiae of the front and middle legs. Amongst the flies, the
pulvilli have adhesive properties, and many beetles have
pads of setae on the underside of the tarsomeres. In each of
these cases the adhesive structures are areas of membra-
nous cuticle covered by large numbers of small setae. For
example in the lady beetle, Epilachna, there are two pads
on the underside of each tarsus. Each pad carries about 800
setae which are 70–120 m long. Many of the setae are
expanded at the tip to form flattened, foot-like structures
Fig. 8.7. Sensory system of the leg. (a) Proprioceptors on the
5–10 m in diameter (Fig. 8.8a). In the fly, Calliphora, the
foreleg of Periplaneta. Numbers in brackets show the number of adhesive setae are also on the tarsi. They are much smaller
sensilla in each group. Ellipses show orientations of campaniform than those in the beetle, only 9–15 m high with a ‘foot’
sensilla. (b) Exteroreceptors on the fore tarsus of the about 1 m in diameter. The fly has about 42 000 adhesive
grasshopper, Schistocerca americana. Posterior view: there are 140 hairs altogether. The flexibility of the setae enables them to
long mechanosensitive sensilla and 200 small chemosensitive make contact with irregular surfaces much more efficiently
sensilla on the upper surface and sides of the tarsus. Ventral view: than would be true of a single, larger structure. This
sensilla on the pulvilli and arolium. There are 180 sensilla. About greatly increases the power of adhesion. The males of
60% are chemoreceptors. many species of beetle have more adhesive setae than the
females. These additional setae are used by the male to
grasp the female during mating.
Hairless adhesive pads occur in a number of insects.
The arolia of cockroaches and grasshoppers can function
MODIFICATIONS OF THE BASIC LEG STRUCTURE 157
Fig. 8.8. Adhesive pads. (a) Tip of tenent hair of Philonthus (Coleoptera, Staphylinidae) (after Stork, 1983). (b) Suckers on the foreleg of
male Dytiscus (Coleoptera, Dytiscidae) (after Miall, 1922).
Fig. 8.9. Adaptations of legs. (a) Digging. Foreleg of a larval cicada (after Pesson, 1951). (b) Grasping. Leg of Haematopinus
(Phthiraptera) (after Séguy, 1951). (c) Grooming. Foreleg of a mutillid (Hymenoptera) (after Schönitzer & Lawitzky, 1987).
(d) Hind tibia and tarsus of a worker honeybee showing the pollen-collecting apparatus (partly after Snodgrass, 1956).
amongst the Diptera. In some Empididae the middle legs Grooming Insects commonly use the legs or mandibles to
are modified in this way, while in Bittacus (Mecoptera) the groom parts of the body, removing particles of detritus in
fifth tarsomere on all the legs closes back against the fourth the process. The eyes and antennae are often groomed,
to form a grasping structure. and so are the wings. Cockroaches clean their antennae
The ability to hold on is important in ectoparasitic by passing them through the mandibles, which chew
insects. These usually have well-developed claws and the lightly at the surface, but many insects use the forelegs
legs are frequently stout and short as in Hippoboscidae, for this purpose, then cleaning the legs with the
Ischnocera and Anoplura. In the latter two groups, the mandibles. Neuroptera and Diptera hold an antenna
tarsi are only one or two segmented and often there is only between the two forelegs, which are drawn forwards
a single claw which folds against a projection of the tibia to together towards its tip. Mosquitoes have a comb, con-
form a grasping organ (Fig. 8.9b). sisting of several rows of setae, at the distal end of the
MODIFICATIONS OF THE BASIC LEG STRUCTURE 159
fore tibia. The combs are scraped along the proboscis or held in place by the hairs of the pollen basket. On return-
antennae in rapid strokes. In many other insects each ing to the nest, the pollen is kicked off into a cell by the
antenna is cleaned by the ipsilateral foreleg which is often middle legs.
modified as a toilet organ. Schistocerca (Orthoptera) has a
cleaning groove between the first and second pads of the Silk production Insects in the order Embioptera are
first tarsomere. This is fitted over the lowered antenna unique in having silk glands in the basitarsus of the front
and then drawn slowly along it by an upward movement legs in all stages of development of both sexes. The basal
of the head and extension of the leg. In Apis and other tarsomere is greatly swollen, and within it are numerous
Hymenoptera there is a basal notch in the basitarsus silk glands each with a single layer of cells surrounding a
lined with spinelike hairs forming a comb. A flattened reservoir (Fig. 8.10). There may be as many as 200 glands
spur extends down from the tip of the tibia in such a way within the tarsomere, each connected by a duct to its own
that when the metatarsus is flexed against the tibia the seta with a pore at the tip through which the silk is
spur closes off the notch to form a complete ring (Fig. extruded.
8.9c). This ring is used to clean the antenna. First it is
closed round the base of the flagellum and then the Reduction of legs Some reduction of the legs occurs in
antenna is drawn through it so that the comb cleans the various groups of insects. For example, among butterflies,
outer surface and the spines on the spur scrape the inner adults of many species have reduced anterior tarsi, and the
surface. A similar, though less well-developed organ, Nymphalidae are functionally four-legged with the front
occurs in Coleoptera of the families Staphylinidae and legs being held alongside the thorax. In male nymphalids,
Carabidae. Lepidoptera have a mobile lobe called the the tarsus and pretarsus of the foreleg are completely
strigil on the ventral surface of the fore tibia. It is often lacking, while in females the fore tarsus consists only of
armed with a brush of hairs and is used to clean the very short tarsomeres. In the male of Hepialus
antenna and possibly the proboscis. (Lepidoptera), on the other hand, the hind leg lacks a
The hind legs of Apoidea are modified to collect pollen tarsus.
from the hairs of the body and accumulate it in the pollen More usually, reduction of the legs is associated with a
basket. Pollen collecting is facilitated by pectinate hairs sedentary or some other specialized habit, such as burrow-
which are characteristic of the Apoidea. In the honeybee, ing, in which legs would be an encumbrance. Thus female
Apis, pollen collected on the head region is brushed off coccids are sedentary and are held in position by the stylets
with the forelegs and moistened with regurgitated nectar of the proboscis. The legs are reduced, sometimes to
before being passed back to the hind legs which also simple spines, and in some species they are absent alto-
collect pollen from the abdomen using the comb on the gether in the later stages of development. Female
basitarsus (Fig. 8.9d). The pollen on the combs of one Psychidae (Lepidoptera) show varying degrees of leg
side is then removed by the rake of the opposite hind leg reduction, some species being completely apodous. These
and collects in the pollen press between the tibia and insects never leave the bags constructed by their larvae.
basitarsus. By closure of the press, pollen is forced out- Legs are also completely absent from female Strepsiptera,
wards and upwards on to the outside of the tibia and is which are parasitic in other insects.
160 LEGS AND LOCOMOTION
Apart from the Diptera, all the larvae of which are cuticle and produce reflex responses in muscles tending to
apodous, legless larvae are usually associated with particu- alleviate those strains. Some campaniform sensilla at the
lar modes of life. There is a tendency for larvae of leaf- proximal end of the tibia of P.americana are oriented paral-
mining Lepidoptera, Coleoptera and Tenthredinoidea to lel with the long axis of the leg, others are at right angles to
be apodous (see Hering, 1951). Parasitic larvae of it (Fig. 8.7a). Axial forces, such as would be produced by
Hymenoptera and Strepsiptera are apodous, and in larval the weight of the insect when it is standing still, are per-
Meloidae (Coleoptera) the legs are greatly reduced. ceived by the most proximal, transversely oriented sensilla,
Finally, in the social and semisocial Hymenoptera in which although their responses to such axial forces are relatively
the larvae are provided with food by the parent, apodous weak. Bending the tibia, however, produces strong
forms are also the rule. responses. When the insect is standing on a horizontal
Review: Schönitzer & Lawitzky, 1987 – antenna cleaners surface with the tibia inclined away from the body, the
mass of the body will tend to cause an upward bending of
the tibia, compressing the proximal sensilla (Fig. 8.11b).
8.3 MAINTENANCE OF STANCE
Twisting the tibia causes both groups of sensilla to
Even standing still requires muscular activity and the con- respond. Stimulation of the proximal sensilla excites slow
tinual adjustment of this activity to compensate for small motor neurons to the extensor tibiae and extensor
shifts in position. Some leg muscles, like the extensor trochanteris muscles, and inhibits the slow motor neurons
tibiae muscles of the front and middle legs of Schistocerca, to the flexor tibiae and flexor trochanteris muscles (Fig.
are continuously active in a stationary insect. Slow axons 8.11c). Stimulation of the distal sensilla has the opposite
innervating these muscles fire at low rates, 5–30 Hz, their effect (Zill, Moran and Varela, 1981). A comparable reflex
activity varying with leg position. The fast axons are not system compensates for stress in the trochanter of the stick
active in a stationary insect, and the inhibitory neurons are insect, Carausius morosus, when the femur is bent anteri-
only sporadically active, but do fire in response to contact orly or posteriorly. Here there are two groups of campani-
or vibration. form sensilla on the trochanter which reflexly activate the
When an insect is standing still, any force tending to retractor or protractor muscles of the coxa (Schmitz,
change the angles between the segments of the legs, such 1993). The pathways between proprioceptive sense cells
as a sudden gust of wind, is opposed by a muscular reflex, and motor neurons are, in some cases at least, monosyn-
called the postural position reflex, and in most cases this is aptic (Skorupski and Hustert, 1991). Similar systems for
mediated by the chordotonal organs. Most studies have the control of stance are almost certainly present in all
examined the femur–tibia joint. In this case, any tendency insects.
to reduce the angle between the femur and tibia is opposed The hair plates on the legs contribute to the insects’
by the tibial extensor muscle, while an increase in the angle gravitational sense (section 23.1.3.2).
is opposed by the tibial flexor muscle.
Similar reflexes have been described at other joints of
8.4 LOCOMOTION
the leg. These reflexes are produced in response to passive
changes in the angles between segments whatever the Mobility at some stage of the life history is a characteristic
initial degree of flexion or extension, but the input from of all animals. They must move in order to find a mate, to
the chordotonal organ, and the activity of the motor disperse and, in many cases, to find food. The success of
neurons to the muscles, varies according to the position. insects as terrestrial animals is in part due to their high
When Locusta migratoria is standing on a horizontal degree of mobility arising from the power of flight (see
surface, the angles between the femora and tibiae of the Chapter 9), but more local movements by walking or
front and middle legs are usually close to 90 °. In the hind swimming are also important.
legs, the angle is more variable, but is usually less than 45 °.
The postural resistance reflexes contribute to the mainte- 8.4.1 Walking and running
nance of these positions in the middle and hind legs, but Most insects move over the surface of the ground by
not in the forelegs (Field and Coles, 1994). walking or running. The legs move in sequences which are
Campaniform sensilla on the legs monitor strains in the varied at different speeds in such a way that stability is
LOCOMOTION 161
usually maintained. Co-ordination of these movements Promotion – the movement of the coxa resulting in
involves central mechanisms, but segmental reflexes are protraction.
also important. Retraction – the backward movement of the leg relative
Reviews: Delcomyn, 1985; Hughes and Mill, 1974 to its articulation between the time the foot is placed on
the ground and the time it is raised.
8.4.1.1 Movements of the legs Remotion – the corresponding movement of the coxa.
In describing the movements of the legs the following Adduction – the movement of the coxa towards the
terms are used (Hughes, 1952): body.
Protraction – complete movement forwards of the Abduction – the movement of the coxa away from the
whole limb relative to its articulation with the body. body.
162 LEGS AND LOCOMOTION
Levation – the raising of the leg or a part of the leg, part axis of the insect. When it has passed this position it exerts
of protraction. a strut effect which, aided by leg extension, tends to push
Depression – lowering the leg, or a part of the leg. the insect forwards.
During protraction the leg is lifted and flexed so that it
Extension – an increase in the angle between two seg-
exerts no forces on the body. The coxal promotor muscle
ments of the leg.
probably starts to contract before retraction is complete, so
Flexion – a decrease in the angle between two segments the change over from retraction to protraction is smooth.
of the leg. As the foreleg swings forwards it extends again, so that in
each cycle of movement the intrinsic muscles undergo two
8.4.1.2 Mechanism of walking phases of contraction and relaxation, while the extrinsic
A leg may act simply as a strut with the forces acting down it muscles only contract and relax once.
depending on its angle of inclination to the body and the The mid and hind tarsi are always placed on the ground
weight of the insect (Fig. 8.12a). Equal and opposite forces behind their coxae, so their longitudinal strut effect always
will be exerted by the leg on the body. The force acting down assists forward movement (Fig. 8.13). The main pro-
the leg can be resolved into two components, horizontal and pulsive forces of both pairs of legs are derived from exten-
vertical, and because the leg is splayed out lateral to the body sion of the trochanter on the coxa and of the tibia on the
the horizontal force can be resolved into longitudinal and femur pushing the insect forwards.
transverse components (Fig. 8.13). The relative sizes of the The longitudinal forces produced by these movements
longitudinal and transverse components will vary according are generally such that the insect moves forwards. At the
to the leg’s position. In Fig. 8.13 it is assumed that only three same time lateral forces are produced and when, for
legs are on the ground (see below) and it is clear that for most instance, the right foreleg is on the ground it tends to push
of its movement the strut effect of the foreleg tends to retard the head to the left. This is partly balanced by the other
forward movement (longitudinal thrust forwards), while legs, but there is some tendency for the head to swing from
that of the middle and hind legs promotes forward move- side to side during walking (see Hughes, 1952).
ment (longitudinal thrust backwards). So long as all the The precise functions of a muscle or a leg during loco-
opposing longitudinal (forwards, backwards) and lateral motion vary with the orientation of the insect. For
(left, right) forces balance each other there will be no move- instance, when Carausius (Phasmatodea) is walking on a
ment, but if the forces are not balanced the body will be dis- horizontal plane, the middle and hind legs provide most
placed due to a fall in the center of gravity. support and most of the propulsive force is provided by the
A leg can also act as a lever, that is a bar on which external hind legs; the forelegs have a largely sensory function.
work is done so that it rotates about a fulcrum. This effect is However, if the insect is suspended beneath a surface, all
produced by the extrinsic muscles which move the leg rela- the legs are used to hold on and much of the power for
tive to the body and so lever the insect along (Fig. 8.12b). movement comes from the middle legs.
The leg, however, is not a simple, rigid strut or bar. It
has intrinsic muscles which can also exert forces on the 8.4.1.3 Patterns of leg movement
body by flexing or extending the leg. If a leg is extended Each step comprises a period of protraction, when the leg
anteriorly, flexion of the joints will pull the body forwards is swung forwards with the foot off the ground, and a
(Fig. 8.12d), while, in a leg directed backwards, straight- period of retraction, as the leg moves back relative to the
ening the joints will push the body forwards (Fig. 8.12c). body with the foot on the ground. The pattern of stepping
When Periplaneta starts to move, the foreleg is fully often varies with the speed of movement. At the lowest
protracted due to maximum coxal promotion and exten- speeds, the insect may have most of its feet on the ground
sion of all the leg segments. At this stage it exerts a strut most of the time and the legs are protracted singly in the
action retarding forward movement. Retraction begins by sequence R3 R2 R1 L3 L2 L1 R3 etc. (where R and L indi-
coxal remotion which produces a lever effect drawing the cate right and left, and 1, 2 and 3 the fore, middle and hind
animal forwards, an effect which is added to by flexion of legs respectively) (Fig. 8.14a) or more irregularly. At
the trochanter on the coxa and the tibia on the femur. This higher stepping rates, three legs, the fore and hind legs of
phase continues until the leg is at right angles to the long one side and the middle leg of the other, are lifted more or
LOCOMOTION 163
flexed
flexed
extended
extended
direction of
movememt
Fig. 8.12. Mechanical functioning of leg. (a) A leg acting as a strut. The axial thrust (A) is exerted down the length of the leg
by virtue of the weight of the insect. The size of the axial thrust depends, among other things, on how much of the weight is
borne by the other legs. It can be resolved into vertical and horizontal components (B and C), but because the foot is held by
friction with the substratum it does not move. Instead, a horizontal force (D), equal and opposite to force (C) acts on the body
and, in this case, tends to push it back unless balanced by other forces. (b) A leg acting as a lever. Contraction of the retractor
muscle tends to swing the leg back so that the foot exerts a thrust (E) on the ground. This can be resolved into vertical and
horizontal components (F and G), but since the foot is held still by friction an equal and opposite force (H) acts on the body
pushing it forwards and upwards. (c) Extension of the coxotrochanteral and femoro-tibial joints of the hind leg pushes the
body forwards. (d) Flexion of the coxotrochanteral and femoro-tibial joints of the foreleg pulls the body forwards.
164 LEGS AND LOCOMOTION
Fig. 8.14. Stepping patterns. Diagram showing the disposition of the feet with different protraction time:retraction time
ratios. Thick lines indicate retraction with the foot on the ground, thin lines protraction with the foot in the air (based on
Hughes, 1952)
LOCOMOTION 165
a) stepping frequency
25
Periplaneta
15 Blaberus
10
Fig. 8.15. Stability. Transverse section through the mesothorax
5
of Forficula (Dermaptera) to show the body suspended between
the legs (after Manton, 1953). 0
0 0.5 1 1.5
Some insects are effectively quadrupedal due to the
modification of the fore or hind legs for other purposes. It is b) drag
common for grasshoppers, in which the hind leg is modified 400
Periplaneta
for jumping to use only the anterior two pairs of legs in (25 o )
walking. At high speed, Tropidopola moves the legs of each 300
drag (µN)
segment together in the sequence L1/R1 L2/R2 L1/R1
etc. It maintains stability by using the tip of the abdomen as 200
Periplaneta
an additional point of support. Mantids often walk with the (0o )
forelegs off the ground, with the stepping sequence L3 L2 100 Blaberus
R3 R2 L3 etc., or L3/R2 L2/R3 L3/R2 etc.
0
0 0.5 1 1.5
Speed of movement The speed of movement varies very
greatly from one insect to another, but in general it is
c) power output
higher at higher temperatures. At 25 °C Periplaneta moves
at about 70 cm s⫺1 with top speeds up to 130 cm s⫺1 (see 2
power output (W.kg -1)
0
8.4.1.4 Co-ordination of leg movements 0 0.5 1 1.5
During walking it is probably usual for all three axons that
speed (m.s -1)
innervate each muscle (fast, slow and inhibitory, see above)
to be active. For example, as Schistocerca lifts its fore foot Fig. 8.16. Mechanics of locomotion in Blaberus, slow moving,
off the ground at the beginning of protraction, both the and Periplaneta, fast moving (after Full & Tu, 1990; Full &
fast and slow axons to the extensor tibiae begin to fire (Fig. Koehl, 1993). (a) Stepping (stride) frequency at different speeds.
8.18a). This has the effect of extending the tibia as the leg (b) Drag at different speeds and, for Periplaneta, different angles
swings forwards. The fast neuron stops firing before the of attack. (c) Power output at different speeds. The hatched area
shows the parasitic power exerted by Periplaneta in order to
insect puts its foot down, but the slow neuron keeps firing
overcome drag.
at a moderately high rate through the first half of retrac-
tion. The activity of the inhibitory neuron peaks during
the second half of retraction, when the slow axon is silent antagonistic muscles in the different segments of the leg.
(Burns & Usherwood, 1979; but see Wolf, 1990) In Periplaneta, for example, the levator muscle of the
The alternating movements of protraction and trochanter is active during protraction, lifting the foot off
retraction are the result of regular patterns of activity of the ground (Fig. 8.18b); the trochanter depressor muscle is
166 LEGS AND LOCOMOTION
a) protraction and retraction times according to the nature of the terrain (Duch & Pflüger,
1995). This flexibility involves modulation of the central
600 pattern by input from the proprioceptors and to some
extent also from other mechanoreceptors on the leg. As in
standing, different groups of proprioceptors may be
duration (ms)
400
involved in different processes. For example, as a slowly
walking cockroach puts its foot down at the end of protrac-
200 retraction tion, the proximal campaniform sensilla on the tibia are
stimulated by the dorsal bending of the leg (see Fig. 8.11).
protraction
The slow motor neuron to the extensor tibiae muscle starts
0 to fire soon afterwards and it is probable that the input from
0 5 10 15
the campaniform sensilla influences both the timing and the
b) protraction/retraction rate of firing of the motor neuron. This reduces the degree
of dorsal bending and the proximal sensilla stop firing. If the
1 rate of firing of the slow neuron to the extensor tibiae
ratio (protraction/retraction)
levator of
trochanter
depressor of
trochanter
depressor of
trochanter
The non-spiking interneurons are known to exhibit generates to overcome these forces, as distinct from that
oscillations of their membrane potentials which are syn- which moves it forwards or vertically, is called the para-
chronized with rhythmic bursts of activity in the motor sitic power.
neurons. The source of these oscillations remains Drag (D) is proportional to the density () of the
unknown. fluid in which the insect is moving, its area at right
Reviews: Burrows, 1992, 1996 angles to its direction of movement (its projected area,
S), its drag coefficient (CD), and the velocity of the rela-
8.4.1.5 Forces acting on the body during walking and tive wind (U)
running
When an animal moves through air or water it generates D ⫽ 0.5CDSU 2
mechanical power to move its mass horizontally and verti- The drag coefficient (CD) depends on the shape of the
cally. In walking, and most cases of jumping and swim- organism (a streamlined form presents less resistance than
ming, it generates this power by moving its legs. In flight, an irregular form), its surface texture (a smooth surface
of course, the power is generated by wing movement. presents less resistance than a rough one), and the
Whether the insect is in air or water, it encounters Reynolds number.
forces acting in opposition to its motion. The force acting Reynolds number (Re) is a measure of the relative
in the opposite direction to forward movement is known importance of inertial and frictional forces acting on the
as the drag force. Lift is defined as the force acting at right moving insect
angles to the direction of movement, and is usually
almost vertically upwards. The power that an insect Re ⫽ Vl/
168 LEGS AND LOCOMOTION
L ⫽ 0.5CLSU 2
8.4.2.1 Jumping with legs 100–200 ms, both flexor and extensor muscles contract
Orthoptera and jumping beetles In Orthoptera, Alticini together. There is no movement of the tibia at this time
(flea beetles) and Orchestes (a weevil) the hind femora are despite the much greater power of the extensor muscle
greatly enlarged, housing the large extensor tibiae muscles because the lever ratio between the flexor and extensor
which provide the power for the jump. In all these insects, muscles (f/e in Fig. 8.23) greatly favors the flexor muscle.
the jump results from the sudden straightening of the When the tibia is closed up against the femur, this ratio is
femoro-tibial joint extending the tibia, which is also elon- about 21:1 (Fig. 8.23d). However, as both muscles exert
gate, so that the tarsus is pushed against the substratum parallel forces on the distal end of the femur, this becomes
with great force. distorted and energy is stored in the semilunar processes
The structure of the hind leg, and especially of the (Fig. 8.22). Rapid extension of the tibia occurs when the
femoro-tibial joint, is adapted to permit the development flexor muscles suddenly relax due to the cessation of their
of maximum force by the extensor tibiae muscle, the motor input and to the activity of their inhibitory nerve
storage of the energy they produce, and its rapid release supply (Fig. 8.24). The semilunar process springs back to
resulting in the sudden extension of the tibia. The exten- its relaxed shape so that the femur–tibia articulation moves
sor tibiae muscle consists of a series of short fibers inserted distally at the same time as the extensor muscle pulls the
obliquely into a long, flat apodeme (Fig. 8.21). In head of the tibia proximally. Because of the length of the
Schistocerca, many of the fibers of this muscle are inner- tibia, a small movement of the head of the tibia produces a
vated only by a fast axon (see Table 10.1). Collectively, big movement of the distal end. This mechanical advan-
because of their oblique arrangement, they have a large tage varies with the position of the tibia, but is greatest,
cross-sectional area and can develop a force up to 16 N about 150 :1, at the start of the movement. As a result of
compared with only 0.7 N by the flexor tibiae muscle. Just the force exerted by the distal ends of the two tibiae, the
above the articulation with the tibia, the cuticle of the insect is hurled into the air. The insect’s center of gravity is
femur is heavily sclerotized forming a dark area known as close to the line joining the insertions of the metathoracic
the semilunar process (Fig. 8.22). Beneath the articulation, coxae, so little torque is produced when the legs extend and
the cuticle of the femur is thickened internally to form a the insect moves through the air without rolling. The
process, known as Heitler’s lump, over which the apodeme initial thrust exerted by the tibiae is directly downwards
of the flexor tibiae slides (Fig. 8.23a). because just before the jump the flexed femur–tibia is
Before a jump, the tibia is flexed against the femur by moved so that the tibia is parallel with the ground. In the
the action of the flexor muscle. The axons to the extensor course of extension, however, a backward component
muscle remain silent (Fig. 8.24). Then, after a pause of develops, pushing the insect forwards.
170 LEGS AND LOCOMOTION
trochanter levator
muscles apodeme to
pretarsus
coxa
tibial flexor tibia
muscle
trochanter
depressor trochanter
tarsal depressor
muscle muscle tarsal levator
muscle
pretarsus
tarsus
a) insertion of b) insertion of
semilunar
extensor process extensor
apodeme apodeme
femur
datum datum
point point pull of extensor
muscle
articulation articulation
head of
tibia tibia
Fig. 8.22. Jumping. Specializations of the hind femoro-tibial joint of a locust. Membranous areas stippled, heavily sclerotized
areas black (after Bennet-Clark, 1975). (a) The tibia is flexed, but the extensor muscle remains relaxed. (b) The extensor
muscle contracts at the same time as the flexor muscle. Because the insertion of the extensor apodeme is almost in line with
the articulation, contraction of the extensor muscle causes distortion of the head of the femur, straining the semilunar
process. Notice that the femur has shortened slightly with reference to the datum point which shows the position of the origin
of the extensor apodeme in (a), and the semilunar process is bowed.
Fifth stage larvae of Locusta can make long jumps of up then slowly declines until day 11 before falling sharply on
to 70 cm, reaching a height of 30 cm. However, the dis- the day before the next molt (Katz & Gosline, 1993;
tance jumped by a grasshopper varies with its size. Larger Queathem, 1991).
insects jump longer distances. For example, the longest
jump made by third stage Schistocerca is about 50 cm, but Homoptera In the jumping Homoptera of the families
adults can jump as far as 1 m. Jumping ability also varies Cercopidae, Cicadellidae, Membracidae and Psyllidae, the
within a developmental stage and, in the final larval stage, jump is produced by a rotation of the leg on the coxo-
reaches a maximum about three days after molting and trochanteral joint. Powerful muscles from the furca, pleuron
LOCOMOTION 171
a) distal end
of femur
insertion of X extensor apodeme
extensor apodeme
Y
axis of femur
articulation flexor apodeme
Z
Heitler's
lump
insertion of proximal end
flexor apodeme of tibia
axis of
tibia
b) c)
X extensor apodeme
e extensor apodeme
X Y e axis of femur
axis of femur
Y f f
flexor apodeme flexor apodeme
Z
Z axis of tibia
axis of Heitler's
tibia lump
d)
20
15
lever ratio (f/e)
10
0
0 50 100 150
joint angle ( o)
Fig. 8.23. Jumping. Mechanical relationship between the tibial extensor and flexor muscles of a locust. X shows the position
at which the apodeme of the extensor muscle is attached to the head of the tibia, and Z the position at which the apodeme of
the flexor muscle is attached. Y is the point of articulation of the tibia with the femur (after Heitler, 1974, 1977). (a) Diagram
showing the position of Heitler’s lump and arrangement of the apodemes. The distal end of the femur is shown in outline
(solid line) and the proximal end of the tibia (dotted). (b), (c) Changes in positions of apodemes and their insertions with the
tibia flexed (b) and extended (c). (d) Changes in the lever ratio of the tibial flexor and extensor muscles as the tibia swings
away from the femur. The very high lever ratio (f/e) when the tibia is fully flexed enables the flexor muscle to hold the tibia in
position despite the much larger size of the extensor muscle which is contracting at the same time.
and notum are inserted into an apodeme from the trochanter Siphonaptera The muscles producing the jump of a flea
and the coxa opens very widely to the thorax to permit the are depressors of the trochanter/femur which arise in the
entry of these muscles. In psyllids, the coxa is fused with the thorax. When the femur is raised by the trochanter levator
thorax and the position of the trochanteral articulations is muscle, the insertion of the depressor muscle relative to
altered so as to bring the femora parallel with the trunk. the point of articulation of the trochanter with the coxa is
172 LEGS AND LOCOMOTION
initial kick a)
motor neurons
to extensor flexion pause co-contraction re-flexion
muscle c)
fast mucron
slow
furca flexed
motor neurons dens b) d)
to flexor
muscle
fast
retinaculum
ventral furca
retinaculum extended
manubrium tube
slow
Fig. 8.25. Jumping in Collembola (partly after Denis, 1949). (a)
inhibitory Furca and retinaculum seen from below. (b) Diagram showing
300 200 600 200 the retinaculum holding the dentes. (c), (d) Diagrams of a
collembolan with the furca in the flexed and extended positions.
50
duration of each phase (ms) Jumping is produced by the swing from the flexed to the
extended position.
Fig. 8.24. Jumping. Activity of the motor neurons controlling the
extensor and flexor tibiae muscles of the hind leg of a locust in Other insects Jumping as a result of the sudden release of
relation to a jump. Vertical lines represent action potentials (after
tension previously developed also occurs in Elateridae and
Heitler & Burrows, 1977).
the larvae of various Diptera. Elaterids (click beetles)
jump if they are turned on their backs and the jump serves
such that it compresses a pad of resilin (section 16.3.3) as a means by which they can right themselves. The insect
above the base of the leg without rotating the femur. The first arches its back between the prothorax and the
energy produced is stored in the resilin until a slight mesothorax so that it is supported anteriorly by the pro-
forwards movement of the depressor muscle, produced by thorax and posteriorly by the elytra with the middle of the
a muscle inserted into its tendon, causes the coxa to swing body off the ground (Fig. 8.26). This movement is pro-
suddenly downwards as the tension in the system is duced by the median dorsal muscle and results in the
released. This has the effect of projecting the insect into withdrawal of a median prosternal peg from the pit in
the air (Bennet-Clark & Lucey, 1967). which it is normally at rest. The massive prothoracic
Reviews: Bennet-Clark, 1990 – grasshopper jumping; Burrows, intersegmental muscle acts antagonistically to the median
1996 – grasshoppers, neural control dorsal muscle, but when it starts to contract a small
process on the upper side of the peg catches on a lip on the
8.4.2.2 Mechanisms of jumping not involving legs anterior edge of the mesosternum and no movement
Collembola Collembola jump using modified abdominal occurs. Tension builds up in the muscle because of its
appendages (Fig. 8.25). Arising from the posterior end of continued contraction and energy is stored within it and,
the fourth abdominal segment is a structure called the possibly, in the associated cuticle. Finally, the prosternal
furca, which consists of a basal manubrium bearing a pair peg slips off its catch and this energy is released as rota-
of rami, each divided into a proximal dens and a distal tional energy, both prothorax and the posterior end of the
mucron. The furca can be turned forwards and held flexed body rotating upwards towards each other, and as transla-
beneath the abdomen by a retinaculum on the posterior tional energy, the center of gravity of both parts of the
border of segment three. The jump is produced by the body being moved upwards with considerable velocity
furca swinging back rapidly to the extended position so (Fig. 8.26c). This translational energy carries the insect
that it strikes the substratum and throws the animal into into the air at an initial speed of about 2.5 m s⫺1, the
the air. Movement of the furca is produced by powerful whole jumping action being complete in about 0.5 ms.
longitudinal muscles in the abdomen coupled, in at least This is a relatively inefficient process and only 60% of the
some species, with distortion of the cuticle so that it acts energy expended during the jump is used in lifting the
like a spring (Christian, 1978, 1979). beetle off the ground.
LOCOMOTION 173
c) energy of energy of
translation rotation
prothorax
hind body
kinetic energy (J.10 -4)
prothorax
0.8
hind body
0.6
0.4
0.2
0
controlled by the differences in tension of the muscles usually running right across the ventral surface of a
throughout the body. segment and armed with stiff, curved setae, which may be
Caterpillars typically have, in addition to the thoracic distributed evenly or in rows or patches. Each pad, or
legs, a pair of prolegs on each of abdominal segments three welt, is provided with retractor muscles. In the larva of
to six and another pair on segment ten (see Fig. 15.5). The Musca there are locomotory welts on the anterior edges of
prolegs are hollow cylindrical outgrowths of the body wall, segments six to twelve and also on the posterior edge of
the lumen being continuous with the hemocoel (Fig. segment twelve and behind the anus (see Fig. 15.7f). In
8.27a). An apical area, less rigid than the sides, is known as movement, the anterior part of the body is lengthened
the planta and it bears one or more rows or circles of out- and narrowed by the contraction of oblique muscles,
wardly curved hooks, or crochets, with which the proleg while the posterior part maintains a grip with the welts.
obtains a grip. Retractor muscles from the body wall are Hence the front of the body is pushed forwards over, or
inserted into the center of the planta so that when they through, the substratum. It is then anchored by the
contract it is drawn inwards and the crochets are dis- mouthhooks, which are thrust against the substratum
engaged. The leg is evaginated by turgor pressure when until they are held by an irregularity of the surface and
the muscles relax. On a smooth surface the prolegs can the posterior part moved forwards by a wave of longitudi-
function as suckers. The crochets are turned up and the nal shortening. As a result, the larva exhibits a regular
planta surface is first pressed down on to the substratum sequence of lengthening and shortening (Fig. 8.28)
and then the center is slightly drawn up so as to create a (Berrigan & Pepin, 1995). In soil-dwelling larvae of
vacuum (Hinton, 1955). Tipulidae, Bibionidae and Hepialidae (Lepidoptera), and
Caterpillars move by serial contractions of the longitu- probably in other burrowing forms, the anterior region is
dinal muscles coupled with leg movements starting anchored by the broadening of the body which accompa-
posteriorly and continuing as a wave to the front of the nies shortening.
body. The two legs of a segment, including those on the
thoracic segments, move in synchrony. Each segment is
lifted by contraction of the dorsal longitudinal muscles of 8.5 LOCOMOTION IN AQUATIC INSECTS
the segment in front and its own dorso-ventral muscles,
while at the same time the prolegs are retracted (Fig. 8.5.1 Movements on the surface of water
8.27b). Subsequently, contraction of the ventral longitu- Some insects and other hexapods are able to move on or in
dinal muscles brings the segment down again and com- the film at the surface of water. Aquatic Collembola, such
pletes the forward movement as the legs are extended and as Podura aquatica, sometimes occur on the surface film in
obtain a fresh grip. As the wave of contraction passes for- large numbers. These animals have hydrofuge cuticles
wards along the body at least three segments are in which prevent them from getting wet, but the ventral tube
different stages of contraction at any one time. These pat- on the first abdominal segment is wettable and anchors the
terns are the product of rhythmic activity in the ventral insect to the surface, while the claws, which are also wet-
nerve cord which occurs even in the absence of sensory table, enable it to obtain a purchase on the water. These
input (Fig. 8.27c) although it is probable that this central animals can spring from the water surface using the caudal
control is normally modified by local reflexes involving the furca in the same way as terrestrial Collembola.
stretch receptors (Johnston & Levine, 1996a,b; Weevers, Gerris (Heteroptera) stands on the surface film and
1965). rows over the surface. All the legs possess hydrofuge prop-
Many geometrid larvae have prolegs only on abdominal erties distally, so they do not break the surface film. At the
segments six and ten. These insects loop along, drawing start of a power stroke, the forelegs are lifted off the surface
the hind end of the body up to the thorax and then extend- and the long middle legs sweep backwards producing an
ing the head and thorax to obtain a fresh grip. indentation of the water surface which spreads backwards
In the apodous larvae of cyclorrhaphous Diptera, as a wave (Fig. 8.29). The mesotarsus pushes against the
movement again depends on changes in the shape of the wave giving extra impetus to the forward movement of the
body as a result of muscles acting against the body fluids. insect which continues as a glide as the middle legs pro-
The posterior segments of the body have raised pads tract off the water surface. During retraction, muscles
LOCOMOTION IN AQUATIC INSECTS 175
mesothorax
metathorax
abdominal 1 lat
abdominal 3 pr
lat
abdominal 5 pr
lat
abdominal 7 lat
0 10 20
time (s)
inserted into the coxa and trochanter contract simultane- of one side while the legs of the other, towards which the
ously, most of the power being provided by two muscles insect is turning, remain still.
arising in the mesothorax and inserted into the trochanter. Stenus (Coleoptera) lives on grass stems bordering
These muscles start to contract before the leg begins to mountain streams in situations such that the beetles fall
move and the rapid acceleration of the leg suggests that into the water quite frequently. The beetle can walk on the
some temporary storage of energy in the cuticle might be surface of the water, but only slowly. More rapid locomo-
occurring (Bowdan, 1978). Steering may be achieved by tion is produced following the secretion of chemicals from
unequal contractions of the retractor muscles on the two the pygidial glands opening beneath the last abdominal
sides and fast turning is produced by movement of the legs tergite. Five chemicals are released, of which the most
176 LEGS AND LOCOMOTION
direction of
movement
retraction
rest protraction
(power stroke)
Fig. 8.29. Movement on the water surface. Positions of the legs of Gerris. Arrows show the directions of movement of the legs
relative to the body; insect moving from left to right (after Nachtigall, 1974).
case the hind leg of the opposite side, but out of phase with the
dorsal contralateral middle leg.
hood
Fig. 8.32. Hind leg modifications of aquatic beetles. Structural adaptations and surface area of each part of the leg (after
Nachtigall, 1962). (a) Gyrinus, (b) Acilius.
largely balanced by the opposite lateral thrust of the legs it will tend to rise again (Fig. 8.35). If the driving
contralateral middle leg. Forward thrust is minimal at the movements of the legs are repeated rapidly, before the
beginning and end of each stroke (Fig. 8.34b, leg at A and insect rises very much, the path may be straightened out
C), but when the legs are at right angles to the body the and by controlling the rate of leg movement the insect can
whole of the thrust developed is longitudinal (Fig. 8.34b, dive, move at a constant level or rise to the surface (Fig.
leg at B). It is advantageous if the velocity of the leg is 8.35b). The beat tends to be faster at higher temperatures
greatest at this point and is low at the beginning and end and so movement becomes more uniform as the tempera-
of the stroke so that the lateral forces, which are produced ture rises. In Dytiscus, the buoyancy effect is offset at
mainly during these phases, are kept to a minimum. This higher speeds by using the middle and hind legs alter-
is the case, at least in Acilius and Gyrinus. In the latter the nately, while Hydrophilus achieves the same effect by using
leg is moving most rapidly when it is at an angle of the legs of the two sides out of phase. Hence these insects
90–135 ° to the body. After this the velocity rapidly falls produce a continuous driving force which offsets their
to zero. buoyancy. Amongst water beetles, secretions from the
pygidial glands increase the wettability of the cuticle. This
Buoyancy Many free-swimming insects are buoyant, that may be particularly important in enabling small species to
is, they have lift within the water, because of the air in their break the water surface film.
tracheae and in air stores. When they stop swimming they A few insects, such as larval Chaoborus (Diptera) and
come to rest at the surface of the water in a characteristic Anisops (Heteroptera), can control their buoyancy so that
position which results from the distribution of air stores they can remain suspended in mid water (Teraguchi, 1975).
on and in the body. Most species float head down and
Notonecta (Heteroptera), for instance, rests at an angle of Stability Because insects swimming beneath the surface
30 ° to the surface. As it kicks with its swimming legs this are surrounded by the water and have no contact with a
angle is increased to 55 ° so that the insect is driven down, solid object, they are, like flying insects, subject to
but as it loses momentum during the recovery stroke of the instability in the rolling, pitching and yawing planes (see
180 LEGS AND LOCOMOTION
Fig. 9.33). The dorso-ventral flattening of many aquatic the insect. Acilius can reach 35 cm s⫺1, larger beetles may
insects provides stability in the rolling and pitching attain speeds of 100 cm s⫺1. The larva of Triaenodes only
planes. The control of yawing involves the eyes, antennae moves at about 1.7 cm s⫺1 because of the high drag pro-
and possibly also receptors on the legs, these receptors duced by its case.
acting so that any unequal stimulation as a result of devia-
tion from a straight course is corrected for. In Triaenodes 8.5.2.3 Other forms of swimming
the long case (Fig. 8.30) acts as a rudder, giving some Appendages other than the legs are sometimes used
stability in the pitching and yawing planes. Rolling may be in swimming. Mosquito larvae when suspended from
controlled by the long, outstretched hind legs. the surface film or browsing on the bottom can glide
Swimming movements are maintained by the flow of slowly along as a result of the rapid vibrations of the
water past the head as the insect moves forwards (the mouth brushes in feeding. In Aedes communis this is the
equivalent of the relative wind). This tends to push the normal method of progression. Caraphractus cinctus
antennal flagellum back, but the scape and pedicel are held (Hymenoptera) parasitizes the eggs of dytiscids, which are
at a constant angle. The water movement is probably mon- laid under water. The parasite swims jerkily through the
itored by Johnston’s organ (section 23.2.3.2) which main- water by rowing with its wings, making about two strokes
tains swimming movements in a manner analogous to that per second. Larval Ephemeroptera and Zygoptera move by
which maintains wing movements in a flying insect vertical undulations of the caudal gills and the abdomen,
(section 9.11.4; Gewecke, 1985). while in the larva of Ceratopogon (Diptera) lateral undula-
tions pass down the body from head to tail driving the
Speed The speed of movement depends on the fre- insect through the water (Fig. 8.36a). Many other dipter-
quency with which strokes are made and the lengths and ous larvae flex and straighten the body alternately to either
velocities of the strokes (Gewecke, 1985). Gyrinus can side, often increasing the thrust by a fin-like extension of
swim on the surface at up to 100 cm s⫺1 in short bursts, the hind end. Mosquito larvae, for instance, have a fan of
the hind leg making 50–60 strokes s⫺1. Beneath the dense hairs on the last abdominal segment and as a result of
surface its speed rarely exceeds 10 cm s⫺1. In general, the the lateral flexing of the body move along tail first (Fig.
maximum sustainable velocity increases with the size of 8.36b). The relative density of mosquito larvae is very close
LOCOMOTION IN AQUATIC INSECTS 181
a) surface
power stroke
long axis of drives insect on recovery stroke
body before dive down insect rises due
to buoyancy
b) surface
a) Ceratopogon b) Aedes
The larvae of Chaoborus and other Diptera make similar Fig. 8.36. Swimming by larval Diptera (after Nachtigall, 1965):
movements to those of mosquito larvae. (a) Ceratopogon, (b) Aedes.
182 LEGS AND LOCOMOTION
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(1967). The jump of the flea: A study of in the cockroach Periplaneta americana. thoracic tibiae. Journal of Experimental
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184 LEGS AND LOCOMOTION
Wolf, H. (1990). Activity patterns of Zill, S.N. & Moran, D.T. (1981b). The Zollikofer, C.P.E. (1994). Stepping pat-
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43–55.
9 Wings and flight
[185]
186 WINGS AND FLIGHT
humeral cross- C Sc
vein (h) C+ Rs 1
R1
Rs 1
Sc -
Rs2
Rs 2
R+ Rs - Rs3
M R
MA + Rs 3
Rs4
CuA + MP - Rs 4
radio-medial
M MA 1 cross-vein
CuP - MA1
2A (r-m)
MP2 MA 2 MA2
3A + 1A
MP 1
CuP MP1
2A +
CuA 2
CuA 1 MP2
MP4 MP3
1A + MP3
X CuP MP4
b) CuA 2 CuA1
C R1 MA CuA 1A
convex veins medio-cubital cross-
vein (m-cu)
concave veins
Sc Rs MP CuP
Fig. 9.2. Wing venation. (a) Diagram of wing venation showing the main cross veins and the names of the cells (italicized)
enclosed by the veins. See text for abbreviations. (b) Section at X–X in (a) showing the concave and convex veins with the
depth of pleating greatly exaggerated.
homologous in different groups of insects (see also Behind the leading edge, the wing is often longitudinally
Wootton & Ennos, 1989). corrugated (Fig. 9.2b). This, in itself, confers some degree
In some very small insects, the venation may be greatly of resistance to longitudinal bending, and the elliptical
reduced. In Chalcidoidea, for instance, only the subcosta cross-section of some of the veins (Fig. 9.3b) confers
and part of the radius are present (see Fig. 9.8f). further resistance to vertical bending. The arrangement of
Conversely, an increase in venation may occur by the folds and veins in the hindwing of Orthoptera also limits
branching of existing veins to produce accessory veins or vertical flexibility while facilitating folding (Fig. 9.3c).
by the development of additional, intercalary veins Cross veins are often circular in cross-section (Fig. 9.3e).
between the original ones, as in the wings of Orthoptera. Where flexibility is required the veins are annulated (Fig.
Large numbers of cross-veins are present in some insects, 9.3f) or have short narrow or unsclerotized regions (Fig.
and they may form a reticulum as in the wings of Odonata 9.4b–f).
and at the base of the forewings of Tettigonioidea and
Acridoidea. 9.1.1.2 Wing flexion
The form of an individual vein reflects its role in the The wings flex and twist during flight to maximize the
production of useful aerodynamic forces by the wing as a output of aerodynamic power. As the wing moves down,
whole. On the leading edge of the wing, the longitudinal bending forces act from below, and significant inertial
veins form a rigid spar supporting the wing as it moves forces act on it as it changes direction at the top and bottom
through the air. In Lepidoptera, for example, the subcostal of the stroke. The production of useful aerodynamic forces
vein is circular in cross-section and so is equally resistant requires that the wing remain relatively rigid on the down-
to bending in any direction (Fig. 9.3a), and, in dragonflies, stroke, but exhibits some flexibility on the upstroke.
the cross veins along the leading edge of the wing form Flexion occurs at specific points of the wing and requires
angle brackets which contribute to its rigidity (Fig. 9.3d). breaks or flexibility in the veins at these points.
OCCURRENCE AND STRUCTURE OF WINGS 187
Cu Rs
M
1A
OCCURRENCE AND STRUCTURE OF WINGS 189
veins (Fig. 9.5). The folding results from the structure and
elasticity of the cuticle of the veins (Hammond, 1979).
The wings are sometimes held in the folded position by
being coupled together or fastened to the body. For
instance, in Psocoptera, the costal margin of the hindwing
is held by a fold on the pterostigma of the forewing. The
elytra of Coleoptera are held together by a tongue and
groove mechanism, but they are also held to the body by a
median longitudinal groove in the metathorax which holds
the reflexed inner edges of the elytra. Dermaptera have
rows of spines on the inside edge of the tegmen which
catch on to combs on the metathorax, while many aquatic
Heteroptera have a peg on the mesothorax which fits into a
pit in the margin of the hemelytron. Symphyta have
specialized lobes, the cenchri, on the metanotum which
engage with rough areas on the undersides of the
forewings to hold them in place.
tegmen
hindwing
folded vannal
region
costal margin
of tegmen
third
abdominal
segment
Sc
basal
suture R1
Rs1
Rs2
M
Cu
articulation
with thorax
anal
lobe
wing scale
jugal
lobe
jugal
frenular bristles
bristles
humeral
lobe jugum
humeral humeral
lobe lobe
Fig. 9.12. Wing coupling mechanisms involving the jugal and humeral regions of the wings. All diagrams represent the
mechanisms as seen from below with the attachment to the thorax immediately to the left. Membrane of the forewing with
dark stippling, that of the hindwing with light stippling (after Tillyard, 1918). (a) Primitive mecopteran pattern (Mecoptera,
Taeniochorista). (b) Jugate coupling in a hepialid moth (Lepidoptera, Charagia). (c) Frenate coupling in a female sphingid
moth (Lepidoptera, Hippotion). (d) Frenate coupling in a male sphingid moth (Lepidoptera, Hippotion).
they are so closely associated, the movements of each of In some Trichoptera, only the jugum is present; it lies
the thoracic segments must influence the other. Hence, it is on top of the hindwing and the coupling mechanism is not
impossible for the fore and hindwings to beat completely very efficient. However, the Hepialidae (Lepidoptera)
independently of each other, and, in Orthoptera and have a strong jugal lobe which lies beneath the costal
Odonata, where the wings are not otherwise linked, both margin of the hindwing so that this is held between the
pairs of wings vibrate with the same frequency and with jugum and the rest of the forewing (Fig. 9.12b). This is
the hindwing beat consistently more advanced than the called jugate wing coupling. In Micropterygidae, the
forewing beat (Fig. 9.32; see Brodsky, 1994). jugum is folded under the forewings and holds the frenu-
In the majority of insects the fore and hindwings are lar bristles. This type of coupling is jugo-frenate coupling.
linked anatomically so that they move together as a single Many other Lepidoptera have a well-developed frenulum
unit. This wing coupling may take various forms, but, in which engages with a catch or retinaculum on the under-
many species, it involves lobes or spines at the wing base. A side of the forewing usually near the base of the subcostal
primitive arrangement is found in some Mecoptera of the vein but sometimes elsewhere. This is frenate coupling.
family Choristidae in which there is a jugal lobe at the base Female noctuids, for instance, have from two to 20 frenu-
of the forewing and a humeral lobe at the base of the costal lar bristles and a retinaculum of forwardly directed hairs
margin of the hindwing. Both lobes are set with setae on the underside of the cubital vein (Fig. 9.12c); in the
known as the jugal and frenular bristles, respectively (Fig. male, the frenular bristles are fused together to form a
9.12a), and, although they do not firmly link the wings, single stout spine and the retinaculum is a cuticular clasp
they overlap sufficiently to prevent the wings moving out on the radial vein (Fig. 9.12d). Thysanoptera have the
of phase. wings coupled in a comparable way by hooked spines at
194 WINGS AND FLIGHT
posterior notal
process
axillary 3A
cord
jugal
fold 4A
the base of the hindwing which catch a membranous fold 9.13). The first is in the dorsal membrane and articulates
of the forewing. proximally with the anterior notal process and distally with
Other insects have the wings coupled by more distal the subcostal vein and the second axillary sclerite. The
modifications which hold the costal margin of the hind- second extends to both dorsal and ventral membranes and
wing to the anal margin of the forewing. Hymenoptera articulates ventrally with the pleural wing process (see Fig.
have a row of hooks, the hamuli, along the costal margin of 7.5b) and distally with the base of the radius. It is also con-
the hindwing which catch into a fold of the forewing; nected with the third axillary sclerite, which articulates
Psocoptera have a hook at the end of CuP of the forewing proximally with the posterior notal process and distally
which hooks on to the hind costa; and the forewing of with the anal veins. The third axillary sclerite is Y-shaped
Heteroptera has a short gutter edged with a brush of hairs with a muscle inserted into the crutch of the Y. In
on the underside of the clavus which holds the costal Hymenoptera and Orthoptera, there is a fourth axillary
margin of the hindwing. Homoptera exhibit a variety of sclerite between the posterior notal process and the third
modifications linking the anal margin of the forewing to axillary sclerite. The precise arrangement of the axillary
the costal margin of the hindwing (see Pesson, 1951). sclerites relative to each other and the flexion lines of the
The wings of the Papilionoidea and some Bombycoidea wing is extremely complex and plays a significant role in
are coupled by virtue of an extensive area of overlap changes in wing form during flight (see Brodsky, 1994;
between the two. This is known as amplexiform wing cou- Wootton, 1979).
pling. A similar arrangement is present in some In addition to the axillary sclerites, there are other
Trichoptera, often occurring together with some other plates in the wing base. Connected with the third axillary,
method of coupling. and perhaps representing a part of it, may be one or two
median plates from which the media and the cubitus arise.
At the base of the costa is a humeral plate and often, proxi-
9.4 ARTICULATION OF THE WINGS WITH THE
mal to it, is another plate derived from the edge of the
THORAX
articular membrane and called the tegula. In Locusta this
Where the wing joins the thorax, its dorsal and ventral cut- has been shown to be an important sensory structure
icular layers are membranous and flexible. In these mem- which modulates the basic pattern of wing movements
branes are the axillary sclerites, which transmit (Wolf, 1993, and see below) This may also be true in other
movements of the thorax produced by the flight muscles to insects. It is well-developed in Lepidoptera, Hymenoptera
the wing. Typically there are three axillary sclerites (Fig. and Diptera (Fig. 9.13).
SENSILLA ON WINGS AND THE HALTERES 195
basal
basal plate
lobe
attached a little more ventrally (Gettrup, 1962). These Calliphora there are about 100 sensilla in each group. The
organs have been identified in acridids, gryllids and tet- sensilla of the scapal plate are parallel with the axis which
tigoniids, but not in a gryllotalpid or a blattid. A chordo- passes through the main point of articulation and the
tonal organ is also associated with each wing in Odonata. center of mass of the haltere (indicated as the long axis of
These sense organs are concerned with the control of wing the haltere in Fig. 9.15); those of the basal plate are ori-
movements (section 9.10.3). Insects with asynchronous ented with their long axes at about 30 ° to the axes of the
flight muscles do not have internal proprioceptors con- longitudinal rows in which they are arranged. Near the
nected with the wings. basal plate is a further small group of campaniform sensilla
known as Hicks papillae. These are set below the general
Halteres The hindwings of Diptera are modified to form surface of the cuticle and are oriented parallel with the
halteres, which are sense organs concerned with the main- long axis of the haltere. There is also a single round,
tenance of stability in flight. Each haltere consists of a undifferentiated papilla near the scapal plate. On the
basal lobe, a stalk and an end knob which projects back- ventral surface there is another scapal plate with about 100
wards from the end of the stalk so that its center of mass is sensilla and a group of ten Hicks papillae. These are ori-
also behind the stalk (Fig. 9.15). The whole structure is ented parallel with the long axis of the haltere. Also
rigid except for some flexibility of the ventral surface near attached to the ventral surface is a large chordotonal organ
the base which allows some freedom of movement, while oriented at about 45 ° to the long axis of the haltere. A
the cuticle of the end knob is thin but kept distended by smaller chordotonal organ runs vertically across the base.
the turgidity of large vacuolated cells inside it. The haltere These sensilla react to the forces acting at the base of
is variable in size. In crane flies (Tipulidae) and robber flies the haltere during flight. They perceive the vertical move-
(Asilidae) it is relatively long, exceeding 12% of forewing ments of the haltere and also the torque produced by
length, but in mosquitoes and Cyclorrhapha it is only lateral turning movements of the fly (section 9.11.2).
about 6% of the forewing length.
On the basal lobe of the haltere are groups of campani-
9.6 MUSCLES ASSOCIATED WITH THE WINGS
form sensilla which can be homologized with the groups at
the base of a normal wing. Dorsally there are two large The muscles concerned with wing movement fall, func-
groups of sensilla: the basal and scapal plates (Fig. 9.15). In tionally, into three groups: direct muscles are inserted into
MUSCLES ASSOCIATED WITH THE WINGS 197
Fig. 9.16. Flight muscles of a locust and their innervation. Numbers on each muscle show the numbers of motor axons,
including inhibitory axons, innervating each unit. Dorso-ventral muscles not arising from the coxae have their origins on the
sternum. (a) Indirect flight muscles. Bifunctional muscles that move the wings and the legs are stippled. (b) Direct flight
muscles.
the wing base and their contractions have direct effects on the flexed position. Odonata have two muscles arising
wing movement; indirect muscles moving the wings indi- from the episternum inserted into the humeral plate and
rectly by causing distortions of the thorax; and accessory two from the edge of the epimeron inserted into the axil-
muscles which modulate the wing stroke by changing the lary plate. The relatively large number of direct muscles
shape or mechanical properties of the thorax. For details of (Table 9.1), reflects their role in changing the form of the
the musculature of Odonata see Simmons, 1977; of wing during the wingbeat cycle to provide the precision
Orthoptera: Wilson & Weis-Fogh, 1962; of Diptera: necessary for efficient aerodynamics and steering.
Heide, 1971; Miyan & Ewing, 1985a; and of Lepidoptera:
Kondoh & Obara, 1982; Rind, 1983. 9.6.2 Indirect wing muscles
Reviews: Brodsky, 1994; Kammer, 1985 The indirect wing muscles are usually the main power-
producing muscles for flight. In all insects, wing elevation
9.6.1 Direct wing muscles is produced by indirect dorso-ventral muscles inserted
The direct wing muscles are inserted on to the axillary into the tergum of the wing-bearing segment. There are
sclerites or the basalar and subalar sclerites (see Fig. 7.5) usually several muscles with different points of origin (Fig.
which connect to the axillary sclerites by ligaments. One 9.16). These muscles are not always homologous. In many
muscle, arising on the pleuron and inserted into the third insects they arise on the sternum or the coxae, but in
axillary sclerite, flexes the wing backwards. It is also active Auchenorrhyncha and Psyllidae the tergosternal muscles
in flight, producing some remotion of the wing during are small and are functionally replaced as wing elevators by
both the up and down strokes and, in this way, effecting the oblique dorsal muscles. These arise on the post-
steering (see section 9.11.3). The basalar and subalar phragma and so are normally obliquely longitudinal, but in
muscles commonly consist of several units arising on the groups mentioned the phragma extends ventrally car-
different parts of the pleuron, as well as the sternum and rying the origins of the muscles with it so that they come to
the coxa (Fig. 9.16). Both muscles are involved in wing exert their pull vertically instead of horizontally.
twisting (see below) as well as wing depression. In addi- Wing depression is produced, in most insects, by dorsal
tion, the basalar muscle is involved in wing extension from longitudinal indirect muscles usually comprising five or
198 WINGS AND FLIGHT
six muscle units. These extend from the anterior to the muscles receive input from four putative octopaminergic
posterior phragma of each wing-bearing segment (Fig. neurons, and the subalar muscle has input from five such
9.16). The mode of action of these muscles is illustrated in neurons (Kutsch & Schneider, 1987)
the next section.
Indirect muscles
Depressor muscles Unifunctional levator muscles Bifunctional levator muscles Direct muscles
Order Number (units) Neurons/unit Number Neurons/muscle Number Neurons/muscle Number Neurons/muscleb
Note:
a In some cases the number of units in a muscle is not known so that more than one neuron/muscle may indicate polyneuronal innervation of a single unit, or may indicate a number
dorso-ventral dorso-ventral
muscle - muscle -
basalar relaxed
contracted muscle -
relaxed basalar muscle -
contracted
dorsal longitudinal
muscle - relaxed
dorsal longitudinal
muscle - contracted
dorso-ventral dorso-ventral
muscle - muscle -
contracted relaxed
Fig. 9.17. Muscular basis of wing movements. (a), (b) In an insect, such as a dragonfly, in which the direct wing muscles cause
depression of the wings. (a) Indirect dorso-ventral muscles cause wing elevation. (b) Direct dorso-ventral muscles cause
depression. (c)–(f) In an insect, such as a fly, in which both up and down movements of the wing are produced by indirect
muscles. (c), (d) Cross-sections of the thorax. (e) and (f) Sagittal sections of the wing-bearing segment from the inside
corresponding with (c) and (d), respectively. In (f), contraction of the dorsal longitudinal muscles raises the tergum (as seen
in cross-section in d) and the wing flaps down.
MECHANISMS OF WING MOVEMENT 201
depressed until a process on the underside of the radial pleural muscles attach. Dragonflies have a similar elastic
vein, known as the radial stop, fits into a groove on top of apodeme where the subalar muscle attaches to the subalar
the pleural process. This contact now becomes the pivotal sclerite.
point for further wing depression which results from Elastic forces are also stored as a result of distortions of
wing bending. On the upstroke, these changes are the thorax. It has been widely believed that the lateral
reversed and the dorsal longitudinal muscles are elon- stiffness of the thorax, produced by the sternopleural
gated as the dorsoventral muscles contract. This descrip- articulation and, to a lesser extent, the tergopleural
tion assumes that there is no click mechanism (see articulation, was of major importance. As a result of this
below). lateral stiffness the position of the wings was thought to be
A number of the muscles moving the wings arise in the unstable for much of the stroke and the wings were only
coxae, which are themselves moveable. Whether these stable in the extreme up and down positions. This arrange-
muscles move the legs or the wings appears to be deter- ment is called a ‘click’ mechanism, the wings ‘clicking’
mined by the activity of other muscles and the position of automatically to one of the stable positions once they
the appendages: if the wings are closed the muscles move passed the position of maximum instability. The accompa-
the legs, but in flight, with the legs in the flight position, nying sudden changes in shape of the thorax were believed
the wings are moved. to be essential components of the stretch-activation
system of the asynchronous muscles (section 10.4.2).
9.7.2 Movement due to elasticity However, critical observations of flies suggest that, at
The capacity to store elastic energy and subsequently to least in these insects, a click mechanism does not nor-
release it at high rates is an essential feature of the flight mally occur (Ennos, 1987; Miyan & Ewing, 1985a,b,
mechanism of most insects. At the beginning of a wing 1988; but see Pfau, 1987 for a contrary view). Energy is
stroke (up or down), energy is expended to overcome the stored during both the up and down strokes, probably in
inertia of the wing, while at the end of a stroke the wing the pleural process which is slightly deformed in both
has momentum and must be stopped. Insects store the halves of the stroke, but probably also in other elements
energy derived from this momentum in elastic systems of the wing articulation. Release of this energy contrib-
which may be in the cuticle or in the flight muscles them- utes to both parts of the stroke, but most obviously to the
selves. This energy is then used on the return stroke upstroke. Stretch activation of the synchronous muscles
(section 10.4.4). still occurs, as in the ‘click’ mechanism, but the mecha-
In Schistocerca (Orthoptera), and probably in most nism and timing of stretching are different. The dorso-
other insects, much of the energy involved in the upstroke ventral muscles, producing the upstroke, are activated by
is stored as elastic forces in the pad of resilin which forms the raising of the scutum by the action of the second axil-
the main wing hinge. This is possible because the aero- lary sclerite (see Fig. 9.18). This occurs towards the end
dynamic forces produced at this time act in the same of the downstroke so that the muscles are activated at the
direction as the wing movement so assisting its move- appropriate time. Stretching of the dorsal longitudinal
ment. Thus the muscles have only to overcome the forces muscles, however, occurs throughout the upstroke, and
of inertia of the wing and elasticity of the wing base, and as especially at the beginning. It is inferred that the delay in
a result some 86% of the energy they produce is stored for activation, following stretching, must be sufficient for
use in the downstroke. The elastic properties of this pad the wing to be at or near the top of the upstroke before
are almost perfect and all but 3% of the energy imparted they start to contract (Miyan & Ewing, 1985a). There is
to it when it is stretched during the upward movement of also good evidence that stretch-activation in bees does
the wings is available for pulling the wing down. The not depend on a click mechanism (see Esch & Goller,
radial stop in the wing articulation of cyclorrhaphous 1991).
Diptera (see above) may also enable energy to be stored in In insects with fibrillar muscles it is probable that the
the cuticle at the end of the downstroke. Elastic (resilin) muscles themselves are the principal site of energy storage.
ligaments connect the subalar sclerite to the second and These muscles are characterized by a greater resistance to
third axillary sclerites of Calliphora which also has resilin stretch compared with other muscles due to the elastic
in the apodemes to which the pleuroaxillary and tergo- properties of the contractile system (section 10.4.2).
202 WINGS AND FLIGHT
radial
stop
pleural
process
upward pressure of
scutellar lever
scutum
paranotal
d) plate
first axillary height of scutum
sclerite above pleural
process
wing
second axillary articulation of
sclerite 2nd axillary
sclerite
Orthoptera
Plecoptera synchronous flight
muscles
Neuroptera
Mecoptera
Megaloptera
Trichoptera
Lepidoptera
Psocoptera
Hemiptera
Diptera
wings ‘clapping’ together above the body (see below) and pleural process, it functions as a wing depressor. It may be
are associated with greater power output. They occur most active at any time during the wing stroke, including the
frequently at the beginning of flight, when high lift forces upstroke, but, because of the geometry of its insertion, it is
are necessary to raise the insect off the ground. In most effective when the wing is almost horizontal. At this
Drosophila, an increase in amplitude from 90 ° to 140 ° is point, its action can bend the wing down from the radial
associated with a change in the stroke plane, but in Apis the stop (see Fig. 9.18) and so increase the amplitude.
amplitude varies independently of stroke plane. Variation Amplitude may also be affected by a ‘gear change’ (see
in the amplitude of wingbeat on the two sides of the body above).
may be used in steering, the insect turning away from the
side of greatest amplitude. 9.8.4 Wingbeat frequency
Wings whose primary function is protective, such as Amongst the Odonata and orthopteroid insects, which are
the elytra of beetles and tegmina of grasshoppers, beat usually moderate to large sized, the wingbeat frequency is
with lower amplitudes since they are not the primary usually within the range 15–40 Hz (Fig. 9.21).
power producers. The forewings of Locusta, for instance, Hemipteroid insects usually have higher wingbeat fre-
commonly move through 70–80 ° compared with quencies than this and, in the small whiteflies
110–130 ° for the hindwings, and the elytra of Oryctes (Aleyrodidae), the frequency may exceed 200 Hz.
(Coleoptera) have an amplitude of only about 20 °, nearly Hymenoptera and Diptera commonly beat the wings even
all the power coming from the hindwings. more rapidly, while different species of Lepidoptera have
At least in Diptera, amplitude is largely controlled by wingbeat frequencies ranging from about 4 Hz to 80 Hz.
the activity of the muscle which inserts on to the third axil- Insects with high wingbeat frequencies generally have
lary sclerite. Because it inserts at a point distal to the asynchronous flight muscles.
MOVEMENTS OF THE WINGS 205
Fig. 9.26. ‘Clap and fling’ flight mechanism in a small parasitic wasp (Hymenoptera, Encarsia). Upper row shows an oblique
dorsal view of the movements of the wings with the underside stippled, lower row the cross-section at the midpoint of the
wings. Heavy arrows show wing movements, thin arrows air movements (after Weis-Fogh, 1973).
208 WINGS AND FLIGHT
Fig. 9.27. Vortices round the moving wings (after Grodnitsky & Morozov, 1993). (a) Start of the downstroke. A starting
vortex forms on the upper side of the trailing edge of each wing, as seen in a section of the wing (upper diagram) and from the
front of the insect (lower diagram). (b) Mid–late downstroke. The vortices of the two sides join, remaining attached to the
insect at the wing tips, seen from in front (top diagram) and the side (lower diagrams). Air (arrows) is drawn through the
vortex over the dorsal surface of the insect. (c) At the start of the upstroke, a stopping vortex forms beneath the wing.
Subsequently, the starting and stopping vortices join and are shed behind the insect.
similar ‘clap and peel’ in which the wings ‘peel’ apart, underside of the wing. It is called the stopping vortex; it
starting at the leading edge, also occurs periodically in rotates in the opposite direction to the starting vortex (Fig.
larger insects such as locusts and butterflies. In these cases, 9.27c). On the upstroke it gains in velocity, and the vortices
the phenomenon may be important in generating high lift of the two sides join so that starting and stopping vortices
forces (Cooter and Baker, 1977). form a ring connected to each other and to the wing tips.
Figure 9.27 is an example of the type of airflow develop- Finally, as the wings pronate at the top of the vortex, the
ing round the wings of a larger insect in normal flight. As vortex ring is thrown off backwards. The series of vortex
the wings move apart at the beginning of the downstroke, a rings behind and below the insect, impart a backwards and
flow of air round the trailing edge of the wing creates a downwards flow to the column of air which they surround
vortex, called the starting vortex, on the upper side of the producing an equal and opposite movement of the insect.
wing (Fig. 9.27a). The speed of rotation of this vortex is It might be expected that small insects would use their
accelerated as the wing moves downwards, and the vortex wings as paddles rather than as aerofoils because of their
tubes of the two sides join in the middle, but remain con- low Reynolds number and the consequent greater impor-
nected to the wings at their tips (Fig. 9.27b). Soon after the tance of viscosity of the air (see section 8.4.1.5; Brodsky,
beginning of the upstroke, a new vortex is created on the 1994). There is, however, no evidence of any insects doing
AERODYNAMICS 209
2 insect
insect
weight
weight
(g)(g)
1
liftlift
-1 downstroke upstroke
Fig. 9.28. Variation in lift in the course of a wing stroke of the Fig. 9.29. Hovering. (a) Diagram showing positions of the body
locust (Orthoptera, Schistocerca). The movements of the and the stroke plane adopted by many insects when they hover.
hindwings are shown. The forewings begin their strokes about 0.1 On the anatomical downstroke, the wing is strongly pronated
of a wingbeat later (see Fig. 9.32) (after Cloupeau et al., 1979). (leading edge of morphological upper side indicated by a
triangle). On the anatomical upstroke, the wing is strongly
supinated. Rapid rotations at the end of each half stroke create
this. Even thrips, small Hymenoptera and Diptera appear
the vortex rings shown in (b). (b) Diagram of the airflow round a
to depend on circulatory lift forces (vortices) in the same hovering insect. The vortex rings (shown in section) are thrown
way as larger insects (Ellington, 1984c,d). off below and behind the insect (compare Fig. 9.27). The vortices
Although ‘quasi-steady’ aerodynamic analysis seems draw air downwards as indicated by the arrows. An equal and
inadequate to explain most insect flight, it may be enough opposite reaction supports the mass of the insect (after Ellington,
to account for that of butterflies flying at air speeds in 1984d).
excess of 2 m s1 (Dudley, 1991) and in parts of the
wingstroke of large insects, like locusts, when the wing is and wings through the air, but some is essential in acceler-
moving steadily on the downstroke. This does not mean, ating the air downwards to produce lift. The component of
however, that no non-steady mechanisms are in use. drag which results from lift generation is known as the
Gliding flight (section 9.9.2) is well enough explained induced drag.
by orthodox steady-state aerodynamic theory. Reviews: Brodsky, 1994; Ellington, 1995
Aerodynamic forces acting on the insect: lift, drag and 9.9.1.1 Hovering
thrust The principal function of the wings is to generate Many insects are able to hover. Sometimes this behavior is
lift (section 8.4.1.5). Since the direction of movement of particularly associated with feeding, as in Macroglossum
the wings is constantly changing, so is the direction of lift. (Lepidoptera), or with mating, as in swarms of some flies,
It is reduced on the upstroke and may become negative and it often occurs before landing, enabling the insect to
(Fig. 9.28), but the average lift over the whole wingstroke land precisely on a particular spot.
of an insect is positive, inclined upwards and slightly for- Hovering by many larger insects is achieved with the
wards. Most of the upward component of lift is produced body approaching vertical and the stroke plane almost hor-
by the action of the wings, but a small amount, usually less izontal. The wings rotate through 100 ° or more at the end
than 10% of the total, is produced by the action of the rela- of each half stroke so that their angle of attack is similar on
tive wind on the body, known as body lift. In general, drag the morphologically ‘up’ and ‘down’ strokes (Fig. 9.29). A
is small relatively to the mass of the insect so that the series of vortex rings is produced beneath the insect by the
greater part of the power output is involved in supporting rapid rotations of the wing at the end of each half stroke in
the weight rather than in overcoming drag. the manner shown in Fig. 9.29b (see Ellington, 1984a–f).
Drag results partly from the friction of the air on the However, hovering by hover flies (Syrphidae) and
body and wings, and partly from the kinetic energy given dragonflies is carried out with the body nearly horizontal,
to the vortices which are left behind. Some of this vorticity and presumably involves a different mechanism to produce
is an inevitable consequence of the movement of the body the aerodynamic forces.
210 WINGS AND FLIGHT
150
force (mp)
100
lift
50
0 20 40 60
angle of attack ( o)
b)
150 angle of
30o
o 40o attack
20
60o
50
0o
with scales
o no scales
-5
0
0 50 100 150 200
drag (mp)
9.9.2 Gliding so enable butterflies to glide for longer than would be pos-
Occasionally insects are seen to glide with the wings out- sible without them (Nachtigall, 1976).
stretched. This behavior has been observed in Odonata, During a glide, the insect expends very little energy
Orthoptera and Lepidoptera and ranges from a pause in and it is suggested that the inability of dragonflies to fold
wing movement lasting only a fraction of a second, to pro- their wings is a secondary adaptation to gliding. Locusts
longed glides lasting many seconds. The ability to glide are able to lock their forewings in an outstretched position
depends on the maintenance of a high lift/drag ratio pro- (Neville, 1965) and this may facilitate gliding. Short glides
duced by having the wings at a suitable angle to the relative by Locusta are described by Baker and Cooter (1979).
wind. As the angle of attack is increased, both lift and drag
increase, but above about 35 ° lift starts to decrease while 9.10 CONTROL OF WINGBEAT
drag continues to increase (Fig. 9.30). For various
Lepidoptera, the lift/drag ratio is maximal at an angle of 9.10.1 The initiation of wing movements
attack between 5 and 15 °. The scales on the wings are In most insects the wings start to beat as a result of loss of
believed to contribute to the lift but do not affect drag and tarsal contact with the substratum and in the locust this
CONTROL OF WINGBEAT 211
occurs when the insect jumps into the air. When the legs assume the flight position. Diptera hold their legs in the
are touching the ground, movement of the wings is inhib- flight position when their antennae are stimulated in flight.
ited, contact being perceived through the sensilla of the
legs. In the cockroach, hair sensilla on the undersides of 9.10.3 Nervous control of wing movements
the tarsi as well as campaniform sensilla at all the leg joints In locusts, and other insects with synchronous flight
are involved in this inhibition, but only a small subset of muscles, muscle contraction is regulated directly by the
these sensilla is necessary to produce the effect (Krämer & motor neurons: each time a neuron fires, the muscle which
Markl, 1978). This inhibition is overridden in insects that it innervates contracts. The basic pattern of muscular
engage in preflight warmup. contractions involved in the flight of the locust can be pro-
Since fibrillar, asynchronous muscles only oscillate at duced in the complete absence of input from peripheral
high frequency when stretch-activated, the start of flight sensilla. This rhythm is generated by a complex of inter-
in insects with such muscles depends on some mechanism neurons (forming a pattern generator, section 20.5.4),
to initiate the process. In bees, the separate units in the which drive the motor neurons (Robertson & Pearson,
dorso-ventral muscles are stimulated synchronously by 1985). However, the centrally generated rhythm is slower
neural inputs. This results in a muscle twitch of large and different in certain details from that normally required
amplitude, effecting the stretch of the dorsal longitudinal for efficient flight. Inputs from the tegulae and the stretch
muscles which, at about the same time, are activated via receptors at the base of each wing reset the rhythm and
their motor neurons (Esch & Goller, 1991). keep the pattern generator active. The tegulae of the hind-
At least in locusts, but probably also in other insects, wings affect the activity of both fore and hindwings; the
octopamine appears to have an important arousal effect. Its forewing tegulae affect the activity of motor neurons to the
hemolymph titer rises rapidly in the first few minutes of levator muscles (Wolf & Pearson, 1988).
flight. It has a direct effect on the activity of interneurons The axon of a forewing stretch receptor has a complex of
producing the flight pattern (see Fig. 20.8a) and on the branches in all three thoracic ganglia, while that from a
input of the forewing stretch receptor (Fig. 20.8b); it may hindwing stretch receptor has branches in the meso- and
affect the activity of the flight muscles (section 10.3.2), and meta-thoracic ganglia. These branches synapse with den-
it may be responsible for the early mobilization of lipid drites of the flight motor neurons without any intervening
from the fat body before the release of adipokinetic interneurons so that the pathways between sensillum and
hormone (see Orchard, Ramirez & Lange, 1993). effector muscles are monosynaptic. In addition, they
connect with interneurons in the central pattern-generat-
9.10.2 Maintenance of wing movements ing system. The stretch receptors fire close to the time of
The loss of tarsal contact with the substratum is sufficient maximum elevation of the wings, sometimes just after
to maintain the movement of the wings of Drosophila as depression has begun. Elevation of the wing causes the
well as initiating it, but in most other insects flight soon stretch receptors to fire and their input inhibits the activity
stops unless the insect receives further stimulation. This is of motor neurons to the levator muscles and promotes the
provided by the movement of wind against the head. A activity of motor neurons to the depressor muscles (Pearson
wind speed of only 2 m s1 is sufficient to maintain the & Ramirez, 1990). The chordotonal organs associated with
wing movements of Schistocerca and, since this is less than the tegulae, in contrast, start to fire soon after the beginning
the flight speed of the insect, the relative wind produced in of the downstroke and may continue to be active through
flight will provide sufficient stimulus. Air movement is most of the stroke. Their input signals the completion of the
perceived in locusts by hair beds on the face. In Diptera, downstroke, perhaps by monitoring the velocity of the wing
and in the water beetle, Dytiscus, the wind is perceived by movement, and they elicit an immediate upstroke (Wolf,
movements of the third antennal segment relative to the 1993). In this way, the stretch receptors and tegulae control
second, probably involving Johnston’s organ (Bauer & the wingbeat frequency even though the basic rhythm is
Gewecke, 1985). generated within the central nervous system.
These stimuli also result in the legs being drawn up Superimposed on this basic system are inputs con-
close to the body in a characteristic manner. Thus in cerned with the maintenance of steady flight and with
locusts stimulation of the hair beds causes the fore legs to steering. In the locust, about 20 descending interneurons,
212 WINGS AND FLIGHT
Fig. 9.31. Neural control of wingbeat in an insect with synchronous flight muscles. Sensory inputs from the sense organs of
the head and neck affect the activity of interneurons in the brain (open circles), which vary in the selectivity of their
responses. These interneurons have axons extending (descending) as far as the anterior abdominal neuromeres. In each
ganglion (only one is shown) of the flight system, these descending neurons synapse with a premotor interneuron (large open
circle) which also receives input from the proprioceptors at the wing bases. These different inputs modulate the activity of the
premotor interneuron, which is driven or inhibited by the outputs from the pattern generating systems. The premotor
interneuron activates the appropriate motor neuron (stippled) controlling a flight muscle (after Rowell & Reichert, 1991).
with cell bodies in the brain and axons extending as far as interneurons and from proprioceptors associated with the
the fourth abdominal neuromere, are known to be involved wings. They are driven and inhibited by inputs from the
in conveying information from the head to the motor pattern generator, and they output, sometimes directly, to
neurons in the thoracic and abdominal segments. They the motor neurons of the flight muscles (Fig. 9.31) (Rowell
convey information from the compound eyes, the wind- & Reichert, 1991). Basically similar arrays of interneurons
sensitive hairs, the ocelli, the antennae and proprioceptive occur in the anterior abdominal neuromeres to control the
hairs on the neck. Each descending interneuron tends to activity of the abdominal muscles involved in steering.
be most sensitive to one or two of the sensory inputs, The force exerted by a muscle can be increased either
although many also respond to other inputs. Each one also by increasing the number of units which are active or by
tends to respond best to deviations in a particular direc- increasing the strength of the pull exerted by each unit.
tion, for example, changes in the visual field resulting from Although the units of the indirect flight muscles are only
rolling in one direction rather than the other (see Fig. 9.34) innervated by fast axons they contract more strongly if,
(Baader, Schäfer & Rowell, 1992; Rowell, 1989). instead of being stimulated by a single action potential,
Within each of the thoracic ganglia, numerous other they are stimulated by two or more spikes following close
interneurons are involved in steering. In the mesothoracic together (section 10.4.4). This provides a means by which
ganglion of Locusta, there are at least 28 of these neurons, graded information can be transmitted to muscles despite
which are additional to those producing the basic pattern the all-or-nothing code of the nervous system. Thus when
of oscillation. They receive inputs from the descending the insect is producing only low lift forces, the second
CONTROL OF WINGBEAT 213
prothoracic dorsal
longitudinal
basalar 1
basalar 2
mesothoracic subalar
levators
hindwing
mesothoracic dorsal
longitudinal
basalar 1
basalar 2
metathoracic subalar
levators
0 20 40 60 80 100 120
time (ms)
Fig. 9.32. Neural control of wingbeat in an insect with synchronous flight muscles. Diagram illustrating the timing of firing
of motor neurons to the flight muscles of the fore and hindwings of a locust in relation to the wingbeat cycle. Each neuron is
shown by a horizontal line with its origin in the appropriate ganglion on the left-hand side. Each dot on a line represents an
action potential occurring at that time; a small dot indicates that activity in the neuron may or may not occur, a large dot that it
always occurs. The heavy bar on the motor neuron to the forewing subalar muscle indicates that firing occurs within this
period, but not at a precisely fixed time as with the other units. The heavy curves indicate the angular displacement of the
wings (after Wilson and Weis-Fogh, 1962).
basalar muscle and some units of the dorsal longitudinal The problem of control of the wingbeat is different in
muscle of the hindwing may be inactive, whereas in pro- insects in which the wingbeat is produced by asynchro-
ducing high lift forces all the units come into action and nous muscles. Here, too, the muscles act in a precise
the forces exerted by the individual units are increased by sequence, but this sequence is not directly related to
double firing of the motor neurons. In Lepidoptera, nervous input and the timing of firing of the motor
however, each motor neuron produces five to seven action neurons does not coincide with any particular phase of the
potentials in each cycle and the burst length is directly cor- wingbeat cycle. The nervous input to the flight muscles
related with the duration of muscle contraction, and so is serves only as a general stimulator, maintaining the muscle
inversely correlated with wingbeat frequency (Kammer, contractions (section 10.3.2). In general, the motor
1985). neurons only produce single spikes, and their rate of firing
The twisting of the wings by controller muscles in the varies from five to 25 spikes s1 while wingbeat frequency
locust is precisely timed by the pattern of motor impulses is commonly in excess of 100 Hz.
to the muscles (Fig. 9.32). Only in the case of one muscle, Wingbeat frequency in these insects is controlled to
the mesothoracic subalar muscle, is the firing of the motor some extent by the muscles that control the mechanical
neuron very variable in its timing and this is the muscle properties of the thorax; an increase in the lateral stiffness
which varies the twisting of the forewing to control lift. of the thorax produces an increased wingbeat frequency,
The precise co-ordination of the other neurons does not while a decrease in stiffness leads to a reduced frequency.
arise from a fixed pattern of connections between them as There is evidence, however, that the rate of firing of the
some function during walking in sequences completely motor neurons is positively correlated with the wingbeat
different from that involved in flight. frequency (Kammer, 1985).
214 WINGS AND FLIGHT
pitch roll
may be corrected passively through the shape of the body
and form of the wingbeat, but insects also have the capac-
ity to make active changes in the aerodynamic forces
acting on the body in order to maintain a steady flight.
Review: Kammer, 1985
20
10
0
0 5 10 15 20
contrast frequency (Hz)
unusual angles. This might occur, for instance, with the optimized. The information is relayed to the flight control
sun low in the sky just before sunset. The fact that this system in the thoracic ganglia via interneurons some of
does not occur indicates that other stimuli are also impor- which are sensitive to specific types of input. Fig. 9.34a
tant. Schistocerca also orients to the horizon, keeping it shows the firing of such an interneuron in Schistocerca. It
transversely across the eyes with the upper ommatidia responds mostly when the insect rolls strongly to the left,
more brightly illuminated than the lower ones. Orientation but only if there is wind on the head. It barely responds to
to the horizon is accurate and, in good light, the insect can roll to the right.
follow slow changes and even oscillations of the horizon up The dorsal light reaction gives stability to the head, and
to 40 Hz although under these conditions it is unable to deviations from the stable position cause flight steering
stabilize the position of the head. Both the compound eyes responses to restore stability. However, the head may reach
and ocelli are involved in the horizon-detecting response. its stable position before the rest of the body is aligned with
Although fine tuning of the response depends on the com- the head. Any deviation from this alignment is signalled by
pound eyes, the ocelli decrease the latency between a proprioceptors between the head and the thorax. In
change in the horizon and the insect’s response so that the Schistocerca there are hair beds on the cervical sclerite and
rate of stabilization of the image in the compound eye is hairs along the anterior border of the pronotum which are
216 WINGS AND FLIGHT
involved in this orientation. Unequal stimulation of the similar orientation (Fig.9.14), so that each group responds
sensilla on the two sides due to a turning of the thorax rela- maximally to torque in a particular direction and, if the
tive to the head leads to differential twisting of the wings so sensitivity of the sensilla is appropriate, do so only once
that the thorax is brought back into alignment again during a wing cycle. It is very likely that any tendency for
(Taylor, 1981). the insect to deviate from a stable orientation would result
in differential changes in the stimulation of these sensilla,
Pitching When flying steadily, an insect tends to keep the which could thus exert a controlling influence on the
body angle to the horizontal more or less constant. In bum- wingbeat to correct for the deviation. This is certainly the
blebees the body angle is reduced at higher speeds case in the control of lift and pitching in Schistocerca, but
(Fig.9.20d), but Baker, Gewecke & Cooter (1981) did not the situation is best understood in the halteres of Diptera,
observe any correlation between flight speed and body which are specialized organs of stability.
angle in free-flying locusts. The average value for the body
angle was 7.4 °. In the locust, any tendency to pitch is Halteres The halteres vibrate with the same frequency as
counteracted by changes in the twisting of the forewing the forewings, but in antiphase. Their movement is less
during the downstroke so that the forces it exerts are complex than that of the wings. Because of their structure,
modified. There is no regulation of the upstroke or of the with the center of mass in the end knob (Fig.9.15), and
hindwing in any phase. The twisting of the forewing is because of the nature of their articulation with the thorax,
regulated by the campaniform sensilla at the bases of the they vibrate in a vertical or near vertical plane without
wings. The mechanism by which bumblebees control body making the complex fore and aft movements of the wings.
angle, and hence body lift, is not known. Hence the forces acting at the base of the haltere and stim-
In Diptera the halteres are important in controlling ulating the campaniform sensilla are limited to a vertical
pitching, but it is also probable that the eyes and Johnston’s plane when the haltere is oscillating with the insect in
organ in the antenna exert some controlling influence over steady flight, and dorsal and ventral torques oscillate with
the wing movements. the same frequency as the vibration of the halteres. These
torques may be perceived by the sensilla of dorsal and
Yawing Vision plays a part in the control of yaw, but in ventral scapal plates which are oriented parallel with the
locusts the sensilla in the facial hair beds have directional long axis of the haltere.
sensitivity. Oblique stimulation of these sensilla, such as The path of the end knob during vibration represents
occurs during yaw, leads to a change in the form of the an arc of a circle about the long axis of the insect and
wingbeat so that the original orientation is restored. The the haltere may thus be regarded as a gyroscope whose axis
insect may also maintain stability in yaw by actively using of rotation corresponds with the long axis of the insect.
the abdomen as a rudder. In Calliphora, they have an angular rotation of about
50 000 ° s1. As in a gyroscope, the moving halteres
Sensilla at the wing base In the normal vibration of a possess inertia, tending to maintain a fixed orientation in
wing, a twisting-force, or torque, is produced in the cuticle space so that, if the insect rotates about its axes of yaw or
at the wing base. If the wing were to move up and down in a pitch, torques will be produced at right angles to the stroke
vertical plane, only vertical torque would be produced. plane. These torques will vary cyclically through the
Thus with the wing in the up position, the cuticle at the course of each oscillation by the haltere with yaw pro-
base on the upper side would be compressed, while that on ducing maximum torques in both up and down strokes,
the ventral side was stretched, and vice versa with the wing while the torques produced by pitch have a single cycle
in the down position; all the forces would be acting parallel during the stroke (Fig. 9.35) (Nalbach, 1993). Roll also
with the long axis of the wing. But because of the complex- produces torques, but these are in the plane of movement
ity of the wing movement the torque will differ in strength of the haltere and are small relative to the torques pro-
and direction in different parts of the wing stroke. The duced by the normal vibration of the haltere. A fly can
torque is perceived by the sensilla, and particularly the modulate the wingbeat to correct for yaw and pitch with
campaniform sensilla, of the wing base. These are only a single haltere, but both are required for correction
arranged in groups, all those within a group having a of roll. It is to be expected that, normally, information
STABILITY IN FLIGHT 217
-100 -100
d) Coriolis forces
pitch
5 5
yaw
force (10 -8N)
0 0
-5 -5
from the halteres of the two sides is integrated in the short axes, and bending the haltere backwards compresses
central nervous system. the campaniform sensilla of the basal plate, and also stimu-
In yawing, the haltere on the outer side of the rotation lates the chordotonal organ. When the insects rolls, the
will tend to swing back relative to the insect, while that on torques in the two halteres will be in antiphase, while in
the inside will swing forwards (Fig. 9.35a,b). The campan- pitching both halteres are affected in the same way at the
iform sensilla respond to compression forces along their same time, by torques at right angles to the stroke plane.
218 WINGS AND FLIGHT
9.11.3 Steering (section 23.2.3.2). In flight, the antennae are held horizon-
Insects must steer continually while in flight, both to main- tally and directed forwards. Movement through the air
tain stability and to maintain or change direction. In locusts, tends to push the flagellum backwards relative to the
steering may involve differences in wing-stroke amplitude insect, but it compensates for this deflection by swinging
and the degree of wing twisting on the two sides, changes in the pedicel forwards. At higher air speeds the compensa-
the phase relationships of the fore and hind wings, and use tion is greater and so the antennae are pointed more
of the abdomen and the hind legs as a rudder. All or only directly forwards (Fig. 9.36). Johnston’s organ only
some of these activities may be employed at different times. responds to movement, and it is probable that, in flight,
Changes in the wingbeat are also involved in insects where vibrations of the flagellum produced by the flapping wings
the abdomen is too short to be an effective rudder. In flies, stimulate Johnston’s organ. Different scolopidia are stimu-
one wing may remain stationary while the other is actively lated depending on the degree of deflection of the
moving, producing a sharp turn. flagellum and it is probably on this basis that airspeed is
determined (Gewecke, 1974).
9.11.4 Control of flight speed
Flight speed is regulated with respect to movement over
9.12 POWER FOR FLIGHT
the ground, groundspeed, and with respect to the air, air-
speed. Flight demands a great deal of power to lift the insect off
Some insects are known to maintain a constant ground- the ground and drive it forwards. The forces exerted by
speed despite variations in the speed and direction of the flight muscles are in no way unusual, and because of chem-
wind. This response depends on perceiving the apparent ical and mechanical inefficiencies only a small proportion
movement of objects in the visual field as the insect moves of the energy expended by the muscles is effectively avail-
relative to them. It is called an optomotor reaction. A flying able. About 80% of the energy consumed by the muscles is
insect appears to prefer images to pass over the eye from lost as heat, and of the mechanical work performed by the
front to back at a certain moderate speed, the preferred muscles only about one half may be aerodynamically
retinal velocity. If an insect flies downwind, this velocity useful. Consequently only 5–10% of the energy consumed
may be exceeded and the insect turns and flies into the by the flight muscles contributes to flight. The high power
wind. An upwind orientation is maintained only as long as output necessary for flight is achieved by their high fre-
it can make headway against the wind. If the wind is too quencies of contraction.
strong for this to occur, the insect lands. The metabolic rates of insects in flight are often 50–100
Amongst the descending interneurons from the brain times higher than their resting rates. Oxygen consumption,
are some that have the potential for mediating this a measure of metabolic rate, increases linearly with the body
response. In locusts, for example, two such neurons arise weight of the insect (Fig. 9.37). The relationship between
in each side of the brain. They are insensitive to image oxygen consumption in flight and weight is essentially the
movements from back to front, as would occur if the insect same for moths, which have synchronous flight muscles,
was flying backwards, and are most sensitive to movements and euglossine bees, which have asynchronous flight
from front to back across the ventral region of the eye (Fig. muscles (see Casey, 1989; Casey, May & Morgan, 1985)
9.34b). They respond maximally when the contrasting The high metabolic rate depends on the availability of
pattern flickers with a frequency of 10 to 20 per second oxygen, a suitably high muscle temperature, and an abun-
(Fig. 9.34c) (Baader et al., 1992). Thus these neurons dant supply of fuel. The demand for oxygen is met by
convey the type of information needed for the optomotor modifications of the tracheal system (see Fig. 17.4). Insects
response to the wing-regulating organization in the use various behavioral and physiological devices to achieve
thorax. Similar interneurons are present in flies a body temperature at which the flight muscles can func-
(Gronenberg & Strausfeld, 1990,1991) and probably in all tion efficiently (section 19.1).
other flying insects. Connections within the brain are
described in Chapter 20. 9.12.1 Fuels for flight
Air speed is measured and regulated by the antennae, at The fuels providing energy for flight vary in different
least in Apis, Calliphora, some Lepidoptera and locusts insects. Hymenoptera and Diptera commonly use
POWER FOR FLIGHT 219
a) in still air b) with head wind Fig. 9.36. Control of airspeed (after
wind Gewecke, 1974). (a) Position of the
flagellum deflected pedicel corrects and antenna in still air. (b) Changes in the
backwards overcompensates position of an antenna resulting from
by airstream for flagellar deflection
a head wind. Long axis of pedicel
shown as a dotted line. (c) Changes in
antennal antennal the antennal angle of a tethered locust
angle angle associated with increasing wind speed
(equivalent to increasing airspeed of a
xis
body axis
body axis
freely flying insect).
llar a
xis
ra
flage
lla
ge
fla
pedicel
scape
long axis
long axis of pedicel
of pedicel
c)
change in antennal angle ( o)
-5
-10
-15
-20
0 2 4 6
airspeed (m.s -1)
hemolymph.
10 glucose
glucose
0
b) hemolymph
30
concentration (µg.µl -1)
lipid trehalose
20
trehalose
10
0
0 20 40 60 0 20 40 60
time (min) time (min)
relatively large amounts of triacylglycerol in the flight other insects, sugars in the gut, in the crop of Tabanus
muscles (Ward, Candy & Smith, 1982). Beyond the (Diptera) and the honey stomach of Apis, may be con-
muscles themselves, the fat body is the principal store of verted to trehalose immediately after absorption and
fuel. transported directly to the flight muscles.
Reviews: Beenakkers, van der Horst & van Marrewijk, 1985; The oxidation of carbohydrate in insect muscle
Candy, 1989 involves the usual processes of glycolysis and the citric
acid cycle (Figs. 9.39, 9.40). Dihydroxyacetone phosphate
Carbohydrates Carbohydrates in the flight muscles are and glyceraldehyde-3-phosphate are formed in equal
usually the immediate source of energy at the start of amounts from fructose-1,6-diphosphate. They are inter-
flight. In the locust, the muscle concentration of glucose changeable and oxidation can occur either by the direct
starts to decline immediately after flight begins, but, transfer of hydrogen to the electron transfer chain or via
in blowflies, there is a transient increase due to the rapid pyruvate and the citric acid cycle. The latter pathway is
production of glucose from trehalose (Fig. 9.38). advantageous because it results in the conservation of a
Subsequently, after about 30 minutes flight, the glucose greater amount of energy as ATP. Consequently, a system
concentration stabilizes in both species. These stable levels favoring the conversion of glyceraldehyde-3-phosphate to
indicate that glucose is provided from other sources, ini- dihydroxyacetone phosphate is desirable. However, the
tially from glycogen in the muscle itself, and then from oxidation of glyceraldehyde-3-phosphate is limited by
elsewhere. the availability of nicotinamide adenine dinucleotide
Trehalose in the hemolymph forms an important car- (NAD).
bohydrate reserve in many insects, and is also the form in Regeneration of NAD from NADH is achieved in the
which carbohydrates are transported from other sites. As a glycerol phosphate shuttle (Fig. 9.40). This involves the
result, the hemolymph concentration of trehalose may fall, transfer of hydrogen to the electron transfer system via
as it does in the locust, where it becomes stable after about dihydroxyacetone phosphate and glycerol-3-phosphate.
30 minutes of flight. In the fly, Calliphora, however, the However, the electron transfer system is in the mitochon-
concentration first rises and then returns to its original dria, while glycolysis occurs in the cytosol. The shuttle
level. The stable levels in both species result from the syn- involves the transfer of glycerol-3-phosphate into the
thesis of trehalose from glycogen in the fat body. In some mitochondria and the movement of dihydroxyacetone
POWER FOR FLIGHT 221
Fig. 9.39. The citric acid cycle and terminal oxidation in the mitochondria. Notice how the glycerol phosphate shuttle, which
channels virtually all carbohydrate metabolism via pyruvate (see Fig. 9.40), results in the greatest production of ATP. Bold,
curved arrows show energy conserving steps. Fatty acids are introduced into the citric acid cycle via acetyl-coenzyme A.
222 WINGS AND FLIGHT
Fig. 9.40. The glycerol phosphate shuttle. Enzymes referred to in table 9.2 are shown in italics. The points at which they are
active are indicated by broken arrows.
phosphate out again. The interconversion of glycerol–3- for muscle contraction. The activity of the flight muscles is
phosphate and dihydroxyacetone phosphate is catalyzed by entirely aerobic and the enzyme lactate dehydrogenase is
the enzyme glycerol phosphate dehydrogenase which is present at very low levels. By contrast, in leg muscles, the
present in the cytosol and in the mitochondria (shown in level is more than 30 times higher.
Fig. 9.40 and Table 9.2 as glycerol-3-phosphate dehydro-
genase in the cytoplasm and glycerol-3-phosphate oxidase Lipids Insects engaging in long-range migration, such as
in the mitochondria). The level of the enzyme in the cyto- locusts, some butterflies and planthoppers switch from
plasm of flight muscle is consistently greater than that in using carbohydrates as the main source of fuel to using
the mitochondria. This limits the rate at which hydrogen is lipids. This switch occurs some 15–30 minutes after take-
transferred to the electron transfer chain by this route, but off and, in general, the lipids are obtained from the fat
it ensures that the catalytic amounts of dihydroxyacetone body where they are stored as triacylglycerides. They are
phosphate required to regenerate NAD are available. transported through the hemolymph as diacylglycerides
Glyceraldehyde-phosphate dehydrogenase (producing and their concentration increases and then stabilizes in the
1,3-diphosphoglycerate) is present in large amounts, espe- first 2–3 hours of flight (Fig. 9.38b).
cially in those insects where carbohydrates form the princi- At the flight muscles, the glycerides are degraded in a
pal flight fuel (Calliphora in Table 9.2). This system series of steps into two-carbon units. Mitochondrial mem-
ensures that virtually all the carbon derived from the origi- branes are impermeable to fatty acids, and transfer of fatty
nal substrate, glucose-6-phosphate, passes via pyruvate to acids into the mitochondria is facilitated by carnitine, a
the citric acid cycle and the enzymes of this pathway are water-soluble vitamin. Within the mitochondria, the fats
present at high levels (Table 9.2). This ensures that the enter the tricarboxylic acid cycle as acetyl-coenzyme A,
greatest amount of energy is conserved and made available condensing with oxaloacetate to form citrate. The
Table 9.2. Flight muscle activity of enzymes associated with the utilization of different fuels in flight. Activity of the enzymes in the fat body is given for comparison where
data are available
Insect (Order)
Enzymes of glycolysis
glyceraldehyde phosphate dehydrogenase 69 — 18 30 — 194
lactate dehydrogenase 20.3 — 20.6 20.1 — 0.05
Notes:
Units are mol substrate converted/mg muscle protein/h.
—, o data.
224 WINGS AND FLIGHT
Fig. 9.41. Proline metabolism in flight muscle associated with the utilization of lipids in the fat body. Enzymes referred to in
Table 9.2 are shown in italics. The points at which they are active are indicated by broken arrows. ALATalanine
aminotransferase.
enzymes catalyzing these various reactions are present at 9.12.2 Mobilization of fuel for flight
high concentrations in the muscles of species using lipids The energy sources used by flight muscles are usually
as the primary flight fuels, but are at low levels or absent stored in a form that is not immediately metabolizable and
from species using mainly carbohydrates as well as from is often at some point remote from the muscles.
other tissues of the same species (Table 9.2). Consequently, the mobilization of these reserves must be
coordinated with muscle activity.
Amino acids Oxidation of amino acids may occur to a The nerve impulse that initiates contraction of the
minor extent in the flight muscle of most insects, but, in a flight muscles activates the fibrillar ATPase by the release
few species, proline provides the major substrate oxidized of Ca2 from the sarcoplasmic reticulum. This calcium
by the flight muscles although lipids in the fat body are the also promotes the activation of the phosphorylase involved
ultimate source of fuel. This occurs in the tsetse fly, in the breakdown of glycogen to glucose-1-phosphate and
Glossina, and some beetles, such as Leptinotarsa. The probably of glycerol-3-phosphate dehydrogenase, which is
initial reserve of proline is small, and in the tsetse fly involved in the glycerol phosphate shuttle. As a conse-
sufficient to last only for about two minutes, and it is prob- quence, utilization of carbohydrate proceeds at a fast rate.
able that proline is synthesized during flight. Proline is The mobilization of glycogen in the fat body of locusts
first converted to glutamate, which then undergoes trans- and some flies is regulated hormonally. In locusts, the
amination with pyruvate to produce alanine and adipokinetic hormone (AKH, see below) also mediates
oxoglutarate (Fig. 9.41). The latter enters the citric acid glycogen metabolism by activating a glycogen phosphory-
cycle while the former is returned to the fat body for the lase. In the moth, Manduca, however, AKH does not act in
resynthesis of proline. In the flight muscles, the level of this way. In this species, activation of the glycogen phos-
glutamate dehydrogenase is higher than in other insects, phorylase is regulated by the titer of hemolymph carbohy-
while the level of alanine aminotransferase is high in both drates. A fall in the level of hemolymph trehalose as it is
flight muscle and the fat body (Table 9.2). The activity of utilized by the flight muscles during flight stimulates the
coenzyme A dehydrogenase in the fat body is comparable activation of the enzyme (Ziegler & Schulz, 1986).
with that in the flight muscles of insects oxidizing lipids as In locusts and some other insects, information from the
their primary flight fuel. brain leads to the release of adipokinetic hormone from the
REFERENCES 225
corpora cardiaca, but this release is inhibited if the carbo- muscles (see Fig. 6.11). In locusts the release of diacylglyc-
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tion to its effect on glycogen mobilization, this hormone the start of flight and the concentration more than doubles.
causes the mobilization of lipids in the fat body by activat- It is also possible that octopamine is involved in the early
ing a lipase. Diacylglycerides are released from the fat stages of lipid mobilization (Orchard et al., 1993).
body and these are transported in the hemolymph to the Review: Wheeler, 1989
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mechanism of the blowfly (Calliphora Structure and innervation of the third the direct flight muscles of Drosophila
erythrocephala) in tethered flight. axillary muscle of Manduca relative to melanogaster are morphologically
Journal of Comparative Physiology A, its role in turning flight. Journal of specialized. Journal of Comparative
165, 321–31. Experimental Biology, 131, 373–402. Neurobiology, 340, 427–43.
Nalbach, G. (1993). The halteres of the Rind, F.C. (1983). The organization of Uvarov, B.P. (1966). Grasshoppers and
blowfly Calliphora I. Kinematics and flight motoneurones in the moth, Locusts, vol. 1. Cambridge: Cambridge
dynamics. Journal of Comparative Manduca sexta. Journal of Experimental University Press.
Physiology A, 173, 293–300. Biology, 102, 239–51. Ward, J.P., Candy, D.J. & Smith, S.N.
Neville, A.C. (1965). Energy and Robertson, R.M. & Pearson, K.G. (1985). (1982). Lipid storage and storage
economy in insect flight. Science Neural circuits in the flight system of during flight by triatomine bugs
Progress, London, 53, 203–20. the locust. Journal of Neurophysiology, (Rhodnius prolixus and Triatoma infe-
Norberg, R.A. (1972). The pterostigma of 53, 110–28. stans). Journal of Insect Physiology, 28,
insect wings an inertial regulator of Rowell, C.H.F. (1989). Descending inter- 527–34.
wing pitch. Journal of Comparative neurones of the locust reporting devia- Weis-Fogh, T. (1956). Biology and physics
Physiology, 81, 9–22. tions from flight course: what is their of locust flight. II. Flight performance
Oertli, J.J. (1989). Relationship of wing role in steering? Journal of Experimental of the desert locust (Schistocerca gre-
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take-off flight in temperate-zone Rowell, C.H.F. & Reichert, H. (1985). Royal Society of London B, 239,
beetles. Journal of Experimental Compensatory steering in locusts: the 459–510.
Biology, 145, 321–38. integration of non-phase locked input Weis-Fogh, T. (1973). Quick estimates of
Oldroyd, H. (1949). Diptera. with a rhythmic motor output. In Insect flight fitness in hovering animals,
I. Introduction and key to families. Locomotion, ed. M. Gewecke & G. including novel mechanisms for lift
Handbooks for the Identification of Wendler, pp. 175–82. Berlin: Paul production. Journal of Experimental
British Insects, 9, part 1. Parey. Biology, 59, 169–230.
228 WINGS AND FLIGHT
Wendler, G., Müller, M. & Dombrowski, Wolf, H. & Pearson, K.G. (1988). Wootton, R.J. (1996). Functional wing
U. (1993). The activity of pleurodorsal Proprioceptive input patterns elevator morphology in Hemiptera. In
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Experimental Biology, 182, 229–53.
10 Muscles
[229]
230 MUSCLES
a)
b) c)
Z-disc
H band A band
T
M
Z I band
thin
A filament actin
thick filament
filament
H
T myosin
A
molecules
heads of
Z myosin
molecules
DY
d) e) f)
M
SR T
0.1 m
1 m 0.1 m 0.1 m
Fig. 10.1. Basic structure of a muscle. (a) Electron micrograph of a longitudinal section of part of muscle (asynchronous
flight muscle of the wasp, Polistes). Abbreviations: A ⫽A band, H ⫽H band, I ⫽I band, M ⫽mitochondrion, T ⫽transverse
tubule, Z ⫽Z-disc (after Smith, 1968). (b) Diagram showing the arrangement of the filaments that produces the banding
pattern seen in (a). The filaments are aligned with the bands of two sarcomeres in (a). (c) Diagrammatic representation of the
orientation of the actin (thin) and myosin (thick) molecules in a muscle. (d) Electron micrograph of a dyad (DY).
Abbreviations: M ⫽mitochondrion, SR ⫽sarcoplasmic reticulum, T ⫽transverse tubule (from the flight muscle of a
dragonfly, Celithemis) (after Smith, 1966). (e) Electron micrograph of a transverse section of a flight muscle with a ratio of
thin:thick filaments of 3:1 (after Smith, 1972). (f) Electron micrograph of a transverse section of an intersegmental muscle
with a ratio of thin:thick filaments of 6:1 (after Smith, 1972).
different types of muscle. The arrangement of the fibrils adult (Mizisin & Ready, 1986). Even in muscles not con-
within the fiber varies (see below), but they are always in cerned with flight, the number of fibers may be large. For
close contact with the mitochondria, which are sometimes example, in the coxal depressor muscle of the cockroach,
known as sarcosomes. Periplaneta, there are about 765 fibers in the fifth (out of
A single muscle is made up of a number of fibers, some- ten) larval stage. This number only increases to about 870
times a very large number. For example, the metathoracic in the adult (Nüesch, 1985). In contrast to these numbers,
dorsal longitudinal muscle of the adult grasshopper, the number of fibers in asynchronous flight muscles is
Schistocerca, is made up of over 3000 fibers, and even in a small (see below).
fourth stage larva there are over 500 fibers in this muscle. A The muscle fibers are collected into units separated
tergocoxal muscle in the same insect contains about 50 from neighboring units by a tracheolated membrane, and
fibers in the fourth stage larva and about 400 fibers in the each muscle consists of one or a few such units. For
STRUCTURE 231
example, there are five units in the dorsal longitudinal 10.3c). In muscles which do not oscillate rapidly the mito-
flight muscles of grasshoppers, and three in the tergocoxal chondria generally occupy a much smaller proportion of
muscle referred to above. Each muscle unit may have its the fiber volume (Fig. 10.3e–h) making it possible for a
own independent nerve supply, and is thus the basic con- larger proportion of the fiber to be occupied by the con-
tracting unit of the muscle, but in other cases several tractile elements. The mitochondria may be in pairs on
muscle units have a common innervation and so function either side of a Z-line or scattered irregularly between the
together as the motor unit. fibers. Fibers with abundant mitochondria may be colored
Reviews: Aidley, 1985 – contractile machinery; Maruyama, 1985 pink by the high cytochrome content.
– muscle biochemistry The development of the sarcoplasmic reticulum is cor-
related with the mechanical properties of the muscle, and
10.1.2 Variations in structure in particular with the rates of relaxation of fibers. In
Two broad categories of muscle can be distinguished: muscles which tend to maintain a sustained contraction,
skeletal muscles and visceral muscles. Skeletal muscles are such as the locust extensor tibiae muscle (Fig. 10.3e) and
attached at either end to the cuticle and move one part of the accessory flight muscles of Diptera, it is relatively
the skeleton relative to another. Visceral muscles move the poorly developed. On the other hand, in fast-contracting
viscera and have only one or, commonly, no attachment to synchronous muscles, such as those associated with the
the body wall. Many form circular muscles around the gut sound-producing apparatus of male Neoconocephalus
and ducts of the reproductive system. (Orthoptera) and cicadas, the sarcoplasmic reticulum
Skeletal muscles can be differentiated functionally into comprises 15% or more of the total fiber volume (Fig.
synchronous and asynchronous muscles. Most skeletal 10.3c). A characteristic of synchronous flight muscles,
muscles are synchronous muscles: that is, they exhibit a whether they are tubular or close-packed, is that the dis-
direct relationship between motor neuron activity and tance from the sarcoplasmic reticulum to the myofibrils is
contraction (see section 10.5.2). Asynchronous muscles, short, generally less than 0.5 m and even less in very fast-
which do not have this direct relationship, only occur in contracting muscle. In moths with a high wingbeat fre-
the flight muscles of Thysanoptera, Psocoptera, quency, none of the myosin filaments is more than about
Homoptera, Heteroptera, Hymenoptera, Coleoptera and 10 nm from the nearest element of the sarcoplasmic reticu-
Diptera and in the tymbal muscles of some Cicadidae. lum (Elder, 1975). This close proximity facilitates the
rapid release and resequestration of calcium ions during
10.1.2.1 Synchronous skeletal muscles cycles of contraction and relaxation (section 10.3.2).
The form and arrangement of the fibrils in synchronous In synchronous muscles, the invaginations of the T-
muscles is very variable. Tubular muscles have the system occur midway between the Z-disc and the center of
myofibrils arranged radially round a central core of cyto- the sarcomere. Sarcomere length in many synchronous
plasm containing the nuclei. This arrangement is common muscles ranges from about 3 m to 9 m, but is usually
in leg and trunk muscles and also occurs in the flight only about 3–4 m in flight muscles. The I band usually
muscles of Odonata and Blattodea (Fig. 10.2a). In close- constitutes 30–50% of the resting length of the sarcomere,
packed muscles, on the other hand, the fibrils are only but in situ the extent of muscle shortening may be much
0.5–1.0 m in diameter and are packed throughout the less than this. For instance, the I bands of locust flight
whole fiber; the nuclei are flattened and peripheral. Fibers muscle constitute about 20% of the sarcomere length, but,
of this type occur in some larval insects, in Apterygota and during flight, the muscle shortens by only about 5%. Fiber
in the flight muscles of Orthoptera, Trichoptera and diameter is commonly greater in close-packed muscle than
Lepidoptera (Fig. 10.2b). in tubular muscle; up to 100 m in the former compared
The abundance and arrangement of mitochondria is with 10–30 m in the latter.
related to the level and type of activity of the muscles. In Structurally and functionally, synchronous skeletal
the tubular muscles of Odonata and the close-packed flight muscles form a continuum with slow, or tonic fibers at one
muscles of Orthoptera they are large and numerous, occu- extreme and fast fibers at the other. Slow fibers have little
pying about 40 % of the fiber volume (Fig. 10.3a). This is sarcoplasmic reticulum, the volume occupied by mito-
also true of the muscles which oscillate at high frequencies chondria is relatively large (Fig. 10.3g), and the ratio of
to produce the sounds of cicadas and bush crickets (Fig. thin to thick filaments is high (6 :1). The filaments occupy
Fig. 10.2. Muscle types. Electron micrographs of transverse sections of different muscles. Abbreviations: Ax ⫽axon, BL ⫽basal lamina, F ⫽myofibril, M ⫽mitochondrion,
N ⫽nucleus, SR ⫽sarcoplasmic reticulum, T ⫽transverse tubule, Tr ⫽trachea. (a) Part of a tubular muscle with radial arrangement of myofibrils within each fiber. Opposing
white arrows indicate intercellular space between fibers (flight muscle of dragonfly, Enallagma) (after Smith, 1968). (b) Part of a close-packed muscle fiber. Arrows point to dyads
(after Smith, 1984). (c) Fibrillar muscle showing parts of two myofibrils. Notice their large size (after Smith, 1984). (d) One fiber of visceral muscle. The myofilaments are not
grouped into myofibrils. Arrows point to dyads (spermatheca of cockroach, Periplaneta) (after Smith, 1968).
234 MUSCLES
a) synchronous flight b) asynchronous flight Periplaneta (muscle 136 in Fig. 8.6) consists entirely of fast
muscle muscle fibers. Others include more than one type of fiber. Muscle
60 60
volume (%)
Table 10.1. Fiber types in the extensor tibiae muscle of the locust. The percentages of
muscle fibers having different innervation and ultrastructure
F Fast a, b, c, d, e, f 68
FD Fast b, c, d 26
FS Intermediate a, d, e, f 23
FSI Intermediate a, c, d, e, f 12
FDS Fast a, d 20.5
FI Fast a, d, e, f 22
SI Slow a, f, I35c, I35d 28
S Slow a 20.5
Notes:
After Hoyle (1978b).
* F, fast axon.
* S, slow axon.
* D, octopamine axon.
* I, inhibitory axon.
slow fast
intermediate mixed
surface of each myofibril can be in direct contact with As in other muscles, it consists of thick and thin filaments,
mitochondria. These may be regularly arranged, as presumably representing myosin and actin, often with a
between the Z-discs and H bands in Polistes, or without ring of ten to twelve actin filaments round each myosin
any regular arrangement, as in Calliphora. filament (Fig. 10.1f). A T-system with a regular arrange-
ment is present in Periplaneta, but in Carausius and
10.1.2.3 Visceral muscles Ephestia (Lepidoptera) it is irregularly disposed. The
Visceral muscles differ in structure from skeletal muscles sarcoplasmic reticulum is poorly developed; mitochondria
in several respects. Adjacent fibers are held together by are small and often few in number (Miller, 1975).
desmosomes, which are absent from skeletal muscle, and in The muscles appear striated due to the alignment of
some cases the fibers may branch and anastomose. Further, the filaments. They therefore resemble skeletal muscle but
each fiber is uninucleate and the contractile material is not contrast with the visceral muscle of vertebrates, which is
grouped into fibrils but packs the whole fiber (Fig. 10.2d). not striated. The Z-discs and H bands are irregular and
236 MUSCLES
sarcomere length is very variable. In cardiac muscle, the inserting into the dense material of desmosomes. In asyn-
sarcomeres are short, about 3 m, but they may be as long chronous flight muscle, the terminal region of each
as 10 m in other visceral muscles. myofibril consists of a dense body of microfibers, perhaps
Visceral muscles may be innervated from the stomod- made up of extended actin filaments. Each of these regions
eal nervous system or from the ganglia of the ventral nerve is inserted on to an extension of an epidermal cell contain-
cord, but are sometimes without innervation, as in the ing microtubules as in other muscle attachments (Smith,
heart of Anopheles (Diptera) larvae. 1984).
Reviews: Aidley, 1985; Elder, 1975; Huddart, 1985 – visceral The muscle attachment fibers in the cuticle are not
muscle; Smith, 1984 – ultrastructure digested by molting fluid so that during molting they
retain their attachment to the old cuticle across the exuvial
10.1.3 Muscle insertion space between the new and old cuticles. As a result, the
Skeletal muscles are fixed at either end to the integument, insect is able to continue its activities after apolysis during
spanning a joint in the skeleton so that contraction of the the development of the new cuticle. The connections to
muscle moves one part of the skeleton relative to the other. the old cuticle are broken at about the time of ecdysis (Lai-
Typically such muscles are said to have an origin in a fixed Fook, 1967).
or more proximal part of the skeleton, and an insertion Muscle attachment fibers extending to the epicuticle
into a distal, movable part, but these terms become purely can only be produced at a molt and most muscles appear to
relative where muscles have a dual function (section 9.7.1). form their attachments at this time. Muscle attachment
In many cases, muscles are attached to invaginations of the can occur later, however, if cuticle production continues in
cuticle called apodemes. the postecdysial period, but in this case the attachment
At the point of attachment to the epidermis, the plasma fibers are only connected to the newly formed procuticle
membranes of muscle and epidermal cells interdigitate and do not reach the epicuticle (Hinton, 1963).
and are held together by desmosomes (Fig. 10.5). Within
the epidermal cell, microtubules run from the desmo- 10.1.4 Oxygen supply
somes to hemidesmosomes on the outer plasma mem- Muscular contraction requires metabolic energy, and the
brane, and, from each hemidesmosome, a dense muscles have a good tracheal supply. This is particularly
attachment fiber passes to the epicuticle through a pore true of the flight muscles, where the respiratory system is
canal. In earlier studies, microtubules and attachment specialized to maintain the supply of oxygen to the muscles
fibers were not recognized as separate structures and were during flight (section 17.1.3). In most muscles, the trache-
termed tonofibrillae. In most muscles, actin filaments oles are in close contact with the outside of the muscle fiber.
reach the terminal plasma membrane of the muscle fiber, This arrangement provides an adequate supply of oxygen
STRUCTURE 237
axon
synaptic
vesicles
blood
space
muscle
1 m
axon, but by a separate ‘slow’ axon, usually accompanied neurons from three ganglia. In addition, each side of each
by a second axon. The additional axons may have muscle receives input from an inhibitory cell arising in the
inhibitory or more subtle modulatory effects on the activ- ganglion of its own segment (Fig. 10.8) (Consoulas et al.,
ity of the muscle (see below). 1993)
While it is usual for the different neurons innervating a Sometimes a single neuron innervates more than one
single fiber to have qualitatively or quantitatively different muscle. This is most likely to occur where different
effects, there are examples where this is not so. The trans- muscles commonly act in unison. For example, each of the
verse sternal muscles in the abdomen of the bushcricket, meso- and metathoracic coxae of Periplaneta, has four
Decticus, receive input from three excitatory neurons with depressor muscles (Fig. 8.6). A single fast axon innervates
similar properties (see below) and one of these muscles in all four, although it does not innervate all units in two of
the cricket, Gryllus, is innervated by four neurons with the muscles (135d,e). All the units of two muscles (135d,e)
similar effects (Consoulas et al., 1993). are innervated by a single slow axon, and some are also
Different units of a muscle sometimes serve different innervated by inhibitory axons, one of which goes to most
functions and in this case they have completely separate of the fibers, the distribution of the others being more
nerve supplies. Thus, the posterior part of the basalar restricted. The innervation of sternal muscles in Decticus
muscle of the beetle, Oryctes, is concerned only with wing and in Teleogryllus (Fig. 10.8) is another example of one
depression and has only a fast innervation, but the anterior neuron innervating different muscles, in this case in
part also controls wing twisting and its innervation is different body segments. This arrangement does not mean
complex, consisting of up to four axons, one of which is that activity of the muscles is linked in a fixed way, because
inhibitory. they often receive additional input from separate
The cell bodies of the motor neurons controlling skele- inhibitory neurons.
tal muscles are usually in the ganglion of the segment in Extreme examples of a neuron innervating more than
which the muscle occurs. Sometimes, however, a muscle is one muscle are the common inhibitors in the locust meso-
innervated by a motor neuron with its cell body in a and metathoracic ganglia. These neurons innervate the 12
different ganglion. An extreme example of this occurs in and 13 muscles moving the middle and hind legs, respec-
the abdominal transverse sternal muscles of crickets and tively (Fig. 10.9). These include muscles that normally act
bushcrickets. These muscles are continuous across the antagonistically to each other and which have separate
midline, but the nerve supply of each side is separate. In excitatory innervation. Two other inhibitory neurons in
the bushcricket, Decticus, each side of the muscles in each segment each innervate four muscles in the femur and
abdominal segments 3 to 7 is innervated by excitatory tibia (Hale & Burrows, 1985). Another example of a
CHANGES DURING DEVELOPMENT 239
ventral nerve
trochanter
thorax coxa femur tibia
cord
transverse muscles
segment
nerve 3
segment
cell body in
ganglion
segment
nerve
4
segment
excitatory synapse
inhibitory synapse nerve 5
different segmental ganglia. Muscles of one side only shown; coxal adductor trochanteral depressor
muscles on the other side of the body are similarly innervated.
The complete innervation of the muscle in segment 6 is shown. anterior rotator
Each of the other muscles receives a similar innervation. Some
posterior rotator
neurons innervate muscles in two segments (after Consoulas et
al., 1993).
Fig. 10.9. Innervation of many muscles by a single neuron.
Muscles innervated by the common inhibitor neuron of the
common inhibitor has its cell body in the brain of the
metathoracic leg of a locust. Each rectangle represents a muscle
cricket. It innervates six out of seven antennal muscles with its origin in the segment to the left and insertion in the
(Allgäuer & Honegger, 1993). segment to the right. Nerves 3, 4 and 5 are nerves emanating from
Many of the muscles of the foregut are innervated by the metathoracic ganglion. The axon of the inhibitor neuron has
neurons with cell bodies in the ganglia of the stomodeal a branch in each nerve. Note that the neuron innervates muscles
nervous system. that are antagonistic to each other. Unshaded muscles are those
whose antagonists are not innervated by the neuron (after Hale &
Burrows, 1985).
10.2 CHANGES DURING DEVELOPMENT
Changes occur in many muscles as the insect develops. or with ecdysis, regressing or completely disappearing
During the larval stages, muscles generally increase in size. after a brief period of use. These changes are considered in
At metamorphosis, larval muscles may be destroyed or this section, but see section 15.3.2.2 for changes occurring
modified, or new adult muscles may be developed. at metamorphosis.
Muscles often continue development in the early days of
adult life and this is reflected in the insect’s inability to 10.2.1 Growth during the development of
undertake extended flights during this period. The period hemimetabolous insects
during which an adult insect’s ability to fly is not fully In hemimetabolous insects, muscles increase in size
developed is called the teneral period. Flight muscles may throughout larval development and the increase continues
regress in adults that have completed their flight period. for the first few days after adult eclosion (Fig. 10.10).
Some muscles may be associated specifically with hatching Growth during the larval stages results primarily from an
240 MUSCLES
weight (mg)
indicates the time of adult eclosion.
The period before eclosion includes 5
several larval stadia. (a) Change in wet
weight of the muscle in the cricket,
Teleogryllus (after Ready & Josephson,
1982). (b) Increase in fiber number in 0
the grasshopper, Schistocerca nitens. -40 -20 0 20 40 60 80
(c) Increase in cross-sectional area of days
fibers in the grasshopper, Schistocerca
nitens. (d) Changes in the percentage
b) fiber number c) fiber cross-section
of muscle occupied by mitochondria
and myofibrils in the grasshopper,
Schistocerca nitens. (e) Decrease in 1000
twitch duration in the grasshopper, 3000
area (µm 2)
Schistocerca nitens.
number
2000
Notice that in b–d the final two points 500
represent the mid-point of the last
1000
larval stadium and day 15 of adult life.
For this reason, they do not show 0 0
unequivocally that growth occurred -20 -10 0 10 -20 -10 0 10
after the final molt. Data from other days days
sources, however, show that a marked
increase in fiber cross-section and e) twitch duration
d) volume
changes in the volume densities of the
components do occur in the early
adult (after Mizisin & Ready, 1986).
60 myofibrils 200
time (ms)
% of total
40
mitochondria 100
20
0 0
-20 -10 0 10 -20 -10 0 10
days days
increase in the number of fibers forming the muscles muscle: myofibrils, mitochondria and sarcoplasmic reticu-
whereas growth after eclosion is produced by an increase lum (Fig. 10.10c,d), but the relative rates of increase of
in the size of the fibers. This difference is probably a these components varies from muscle to muscle. In a ter-
reflection of the fact that new attachments to the cuticle gocoxal muscle of the grasshopper, Schistocerca nitens, all
are normally formed at molts (see above). The difference the components increase in proportion during larval
in the number of fibers between early stage larvae and development, but in the metathoracic dorsal longitudinal
adults is relatively small in muscles which perform the muscle the percentage of volume occupied by myofibrils
same functions throughout life, but much more marked in approximately doubles during the last three larval stages.
the case of flight muscles. In both muscles, the proportion of muscle volume occu-
An increase in fiber size involves all the elements of the pied by mitochondria increases during the first two weeks
CHANGES DURING DEVELOPMENT 241
40
glycerol phosphate dehydrogenase
20
lactate dehydrogenase
0
-10 -5 0 5 10 15
days
Fig. 10.11. Enzyme activity in the respiratory pathways in the dorsal longitudinal flight muscle of the locust, Locusta, in
relation to the development of flight behavior. Arrow at day 0 indicates adult eclosion. About seven days after eclosion, the
insect is capable of sustained flight. Enzyme activity is expressed as moles substrate digested per mg muscle protein per
hour. The actual values for lactate dehydrogenase are one-tenth of those shown (after Beenakkers, van den Broek & de Ronde,
1975).
of adult life. Fiber growth in young adults involves an Hymenoptera. This growth involves an increase in the
increase in the size of the myofibrils and, in the dorsal lon- sizes of both mitochondria and myofibrils. In the tsetse fly,
gitudinal muscle of Locusta, a doubling of the number of Glossina, for example, post-eclosion changes comparable
filaments in each fibril (Bücher, 1965; Mizisin & Ready, with those described in Orthoptera occur. In these insects,
1986; Ready & Najm, 1985; Ready & Josephson, 1982). flight muscle maturation is dependent on the insects
These anatomical changes are sometimes accompanied taking several blood meals. The mass of the muscles
by changes in enzyme activity (Fig. 10.11). The activity of increases considerably, mostly due to an increase in the
enzymes involved in flight metabolism increases through absolute size and relative proportion of each fiber occupied
the final stages of muscle development, tending to reach a by the myofibrils (Fig. 10.12). Within each myofibril the
plateau about seven days after the final molt. At the same number of thick filaments more than doubles. The mito-
time, the activity of lactate dehydrogenase declines. chondria also increase in size (Anderson & Finlayson,
1973). At the same time the wingbeat frequency increases,
10.2.2 Post-eclosion growth of the flight muscles of although this is at least partly due to changes in the cuticle.
holometabolous insects Comparable changes have been documented in other flies
At the time of eclosion, when the cuticle expands, the and in the honeybee, Apis, where the mitochondria
flight muscles of cyclorrhaphous flies rapidly increase in undergo a 12-fold increase in volume during the first three
length by 25% or more. The change in length is correlated weeks of adult life. In Lepidoptera, however, no post-
with a comparable increase in the lengths of the sarcom- eclosion changes occur; the flight muscles are fully func-
eres due to an increase in the lengths of the filaments. tional immediately after wing expansion.
Synthesis of the actin and myosin necessary for this
elongation appears to be stimulated by stretching resulting 10.2.3 Regressive changes in flight muscles
from air swallowing during expansion. The number of The flight muscles of the reproductive castes of termites
filaments within a myofibril does not increase at this time and ants regress completely after the nuptial flight, begin-
(Houlihan & Breckenridge, 1981). Similar changes in the ning when the wings are shed. It is believed that the prod-
lengths of flight muscles probably occur in all insects that ucts from the muscles contribute to oogenesis in the period
exhibit a marked increase in body size at eclosion. before workers are available to feed the queen. Flight muscle
An increase in flight muscle volume continues over the degeneration following dealation (casting the wings) also
days following eclosion in cyclorrhaphous flies and some occurs in some crickets (Tanaka, 1993; Walker, 1972).
242 MUSCLES
mesothorax metathorax
60 myofibrils
% of total
40
20 mitochondria
0 coxal
0 5 10 cavity
coxal
cavity apodeme
3
diameter (µm)
spina spina
2
1 b) permanent muscles
0
0 5 10
c) number of filaments
2000
number
1000
0
0 5 10 Fig. 10.13. Molting muscles. Muscles in the pterothorax of a
number of blood meals locust in the first larval stage. Note that the flight muscles are not
Fig. 10.12. Post-eclosion changes in flight muscles of the tsetse well-developed at this time. Membranous areas stippled (after
fly, Glossina. Muscle development is dependent on the insect Bernays, 1972). (a) Muscles which disappear after the final molt.
having several blood meals (after Anderson & Finlayson, 1976). (b) Muscles which remain throughout life.
(a) Percentage of the muscle volume occupied by myofibrils and
mitochondria. (b) Diameter of myofibrils. (c) Number of thick that regulates reproductive development. In Leptinotarsa,
filaments per myofibril. however, the converse is true. Here, the insects enter dia-
pause, and the flight muscles degenerate, when the juve-
In some other insects, flight muscle histolysis follows a nile hormone titer is low; they regenerate when it rises. In
dispersal flight even though the wings are not shed. This is the aphid, Acyrthosiphon, and probably in other insects,
true of some aphid species and other Hemiptera, and in breakdown of the indirect flight muscles is a genetically
some crickets and bark beetles. Amongst bark beetles, such programmed event (Kobayashi & Ishikawa, 1994).
degeneration may be followed, after a period of reproduc- Regression of the flight muscles occurs in older insects
tion, by redevelopment of the muscles, and further flight of many species. This occurs, for example, in some crickets
(see Kammer & Heinrich, 1978). In the Colorado potato (Fig. 10.10a) and in mosquitoes (Aedes) and Drosophila. As
beetle, temporary regression of the flight muscles is associ- the size of the mitochondria declines, so does flight activity
ated with reproductive diapause. (Rockstein and Bhatnagar, 1965; Kammer and Heinrich,
In general, muscle histolysis is correlated with, and 1978).
may be caused by, the increase in juvenile hormone titer Review: Finlayson, 1975
CHANGES DURING DEVELOPMENT 243
tergum 5
10.2.4 Muscles associated with hatching and differentiated only when the insect molts. Within a few
molting days of molting they regress and lose their contractile
Muscles specifically associated with hatching are known to function. They redevelop, in readiness for the next molt,
occur in grasshoppers and crickets. Newly hatched grass- when the insect has a blood meal.
hopper larvae have a pair of ampullae in the neck mem- Amongst holometabolous insects, muscles that func-
brane which are used when the insect escapes from the egg tion only at the time of eclosion are known in Diptera and
shell and makes its way to the surface of the soil. Once the Lepidoptera and they probably also occur in other groups.
insect reaches the surface, the ampullae are no longer used In the blowfly, Sarcophaga, there are special muscles in the
and their associated retractor muscles degenerate. The abdomen that appear to be involved in escape from the
muscles associated with molting (see below) are probably puparium and subsequent cuticle expansion (Fig. 10.14).
also active at this time, but they do not degenerate after These muscles are internal to the definitive muscles and
hatching. In Rhodnius, the muscles that develop at each extend from the front of one presumptive sclerite to the
molt (see below) are also present when the insect hatches, front end of the next so that when they contract the scle-
but regress shortly afterwards. rites buckle because they are not yet hardened, and the
Muscles associated with molting are known from abdominal cavity is reduced in volume. These muscles
several hemimetabolous species and may commonly be break down when the cuticle is expanded and hardened
present. Their function is to facilitate ecdysis and expan- (Cottrell, 1962).
sion of the cuticle at molting by increasing the hydraulic Breakdown of these muscles involves two processes,
pressure of the hemolymph. In grasshoppers, and proba- loss of contractility and muscle degeneration. The first
bly in other insects, some of these muscles are attached to stage, in Lepidoptera, is triggered by the falling
membranous regions of the cuticle and they may prevent concentration of molting hormone. It may begin before
excessive ballooning of these areas so that the greatest eclosion, but the effect is delayed if the motor neurons
forces are exerted on the presumptive sclerites, ensuring controlling the muscles are active (as they normally are at
maximum expansion. Grasshoppers have many of these this time). Under these circumstances, breakdown does
accessory muscles in the neck, thorax and abdomen which not occur until expansion of the adult wings and cuticle is
regress after the final molt (Fig. 10.13). complete, and the first signs of degeneration appear about
In the blood-sucking bug, Rhodnius, some ventral 5 hours after eclosion. In the tobacco hornworm moth,
intersegmental muscles in the abdomen are fully Manduca, the absence of molting hormone accounts for
244 MUSCLES
the complete disappearance of the muscles in the days 10.3 MUSCLE CONTRACTION
after eclosion, but in the silkmoth, Antheraea, eclosion
10.3.1 Mechanics of contraction
hormone provides the signal inducing their final
Muscle contraction results from the thin and thick
degeneration. In the flesh fly, Sarcophaga, eclosion
filaments sliding relative to each other so that each sarcom-
hormone starts a slow degeneration, but some other factor
ere is shortened (Fig. 10.15a). It is believed that actin and
triggers the rapid degeneration of thoracic eclosion
myosin filaments first become linked together by cross-
muscles. The effect of the hormones is to switch on genet-
bridges formed by the heads of myosin molecules and that
ically programmed cell death (Bothe & Rathmayer, 1994;
movement of these links with subsequent breaking and
Kimura & Truman, 1990).
recombination causes the actin filaments to slide further
Review: Truman, 1985
between the myosin filaments so that the sarcomeres, and
hence the muscle, shortens.
10.2.5 Effects of activity on muscles
In most muscles, the extent of contraction appears to be
A few examples are known in which muscle size is affected
limited by the length of the I band. Shortening can con-
by activity. In Glossina, flight following eclosion results in a
tinue only until the end of the thick filaments reach the Z-
rapid increase in the mass of the flight muscles. This
disc, obliterating the I band. However, some body-wall
increase, which occurs more slowly in the absence of
muscles of blowfly larvae and caterpillars and other larvae
induced activity, is due to an increase in the volumes of
with a hydrostatic skeleton are able to supercontract to less
myofibrils and mitochondria (Anderson & Finlayson,
than half of their relaxed length. Intrinsic muscles of the
1976).
gut, heart and reproductive ducts have a similar capacity. In
The hardness of food has been shown to affect the size
these muscles, the myosin filaments pass through pores in
of the mandibular adductor muscles in caterpillars of the
the Z-line and project into the adjacent sarcomeres (Fig.
moth, Pseudaletia. It is not known how quickly the
10.15b). This may be made possible by the cross bridges on
change occurs, but insects feeding on harder food develop
myosin filaments linking with actin filaments of the next
larger heads and larger muscles than those eating soft
sarcomere as they pass through the pores of the Z-disc.
foods. Similar changes in head size and, by implication,
In contrast, some other muscles have the capacity to
muscle development also occur in grasshoppers
superextend. This is true of the intersegmental muscles
(Bernays, 1986).
between segments 4–5, 5–6 and 6–7 in the abdomen of
Flight to exhaustion (which probably rarely occurs nat-
female grasshoppers which extend during oviposition. A
urally) has been shown to affect mitochondrial structure in
single muscle between segments 5 and 6 in Locusta can
the flight muscles of a locust, a wasp and a mosquito. They
vary from 1.2 mm in length when fully contracted to over
become swollen and form a continuous mitochondrial
11 mm when fully extended. This is possible because the
‘mass’ round the myofibrils sometimes to an extent that
Z-discs are discontinuous and fragment into Z-bodies, to
discrete mitochondria cannot be distinguished (Johnson &
which the actin filaments remain attached, when the
Rowley, 1972).
muscle extends (Fig. 10.15c). When the muscles contract
Regression of muscles that are not used also occurs.
after oviposition, the Z-discs may not be completely
This effect is not a direct consequence of lack of use, but is
restored (Jorgensen & Rice, 1983).
controlled indirectly. For example, regression of the dorsal
longitudinal flight muscles of numerous insects following 10.3.2 Control of contraction
loss of the wings is coincident with, and probably con- Muscle contraction results from a series of steps initiated
trolled by, an increase in the titer of juvenile hormone in by the arrival of an action potential at the nerve/muscle
the hemolymph. Grasshoppers have the ability to auto- junction. At an excitatory synapse this leads, first, to
tomize the hind leg, a break appearing between the excitation and then to activation of the muscle fiber.
trochanter and the femur. Muscles in the thorax associated Review: Aidley, 1985
with this leg subsequently atrophy. This is the result of
severing the nerve to the leg even though this nerve does 10.3.2.1 Excitation of the muscle
not innervate the muscles that degenerate (Arbas & With the exception of some visceral muscles, muscles are
Weidner, 1991). stimulated to contract by the arrival of an action potential
MUSCLE CONTRACTION 245
I A band I
H band
actin
Z disc filament
actin
myosin filament
filament
myosin
filament
fenestrated
Z-disc
myosin filament
penetrating
Z-disc
cross-bridges between
filaments of adjacent
sarcomeres
c) superextending muscle
1 2
Z-disc
fragmenting
3 myosin
filament
4
actin
filament
Fig. 10.15. Mechanics of muscle contraction. (a) Normal muscle showing the sliding of the filaments producing shortening
of the sarcomeres (I ⫽I band). (b) Supercontracting muscle. When the muscle is fully contracted, the myosin filaments
extend through perforations of the Z-discs (after Osborne, 1967). (c) Superextending muscle. Numbers indicate successive
stages of extension. When the muscle is extended, the Z-discs become fragmented (after Jorgensen & Rice, 1983).
at the nerve/muscle junctions. Where the junction potential is within the range 30–70 mV, the inside being
involves excitation of a skeletal muscle it is almost certain negative with respect to the outside. Its occurrence
that L-glutamate is the chemical transmitter across the appears to depend largely on maintenance of an excess of
synaptic gap and this may also be true with visceral potassium ions inside the membrane associated with an
muscles (Miller, 1975). As is the case for acetylcholine at a inflow of chloride ions. This distribution is maintained, in
central nervous synapse, the transmitter substance is larval Phormia (Diptera), by a sodium/potassium pump
present in synaptic vesicles at the nerve ending. Some and the passive movement of chloride ions, but in larval
spontaneous discharge of transmitter substance into the Spodoptera (Lepidoptera) by an H⫹/K⫹-ATPase
synaptic gap normally occurs, but the rate of release of the together with a K⫹/Cl⫺ cotransporter system
vesicles is greatly enhanced by the arrival of the action (Fitzgerald, Djamgoz & Dunbar, 1996).
potential (Usherwood, 1974). The arrival of the excitatory transmitter substance at
The unstimulated muscle fiber has a difference in elec- the postsynaptic membrane on the muscle surface causes a
trical potential across the plasma membrane. This resting change in permeability leading to a rise (that is, a
246 MUSCLES
(ms)
duration (ms)
50
membrane potential (mV)
1000
20 20
twitchduration
40
0 0
100
-20 -20 30
twitch
-40 -40 10 20
0 10 20 20 30 40 50
-60 -60 volume
volume (%)
(%) temperature o C)
temperature ((°C)
0 20 40 0 20 40 60
time (ms) time (ms) Fig. 10.17. Twitch duration. (a) Relationship with the degree of
development of the sarcoplasmic reticulum in various insect
Fig. 10.16. Electrical changes at the muscle membrane following muscles (after Josephson, 1975). (b) Effect of temperature in the
stimulation by (a) a fast axon, and (b) a slow axon. Arrows show locust dorsal longitudinal flight muscle (after Neville & Weis-
times of neural stimulation (after Hoyle, 1974). Fogh, 1963).
depolarization) in the muscle membrane potential. The Contractions tend to fuse if the rate of stimulation exceeds
evidence suggests that the inward current producing the ten per second and at 20–25 stimuli per second the muscle
depolarization is carried by calcium ions. The short-lived undergoes a smooth, maintained contraction: it is in a state
increase in potential produced by these changes is called of tetanus.
the postsynaptic potential. The postsynaptic potential A single action potential from the slow axon, on the
spreads from the synapse but decreases rapidly; its effect is other hand, probably releases a small amount of neuro-
therefore localized and large numbers of nerve endings are transmitter and produces only a small postsynaptic
necessary to stimulate the whole fiber (multiterminal potential followed by a very small twitch. With increasing
innervation). frequency of action potentials, the postsynaptic potential
The invaginations of the T-system probably convey the increases in size (Fig. 10.16b) and the velocity and force
changes in potential deep into the muscle and close to the with which the muscle contracts increases progressively;
fibrils. This is important since activation of the fibrils is the response is said to be graded. In the extensor tibiae
dependent on calcium released from the sarcoplasmic muscles of the locust, for instance, less than five action
components of dyads. If the calcium had to diffuse from potentials per second via the slow axon produce no
the surface membrane to the central fibrils there would be response in the muscle, 15–20 Hz produces muscle tonus,
a considerable delay in contraction. The T-system greatly and stimulation by over 70 Hz produces rapid extension
reduces this delay by bringing the plasma membrane to of the tibia. The speed of response increases up to
within a few microns of each fibril. 150 Hz.
The size of the muscle twitch produced by the arrival Review: Pichon & Ashcroft, 1985
of an excitatory action potential depends on the anatomical
characteristics of the muscle fiber and on whether stimula- 10.3.2.2 Activation of the muscle fiber
tion occurs via the fast or slow axons. It must be under- Activation of the contractile mechanism involves the
stood that the terms ‘fast’ and ‘slow’ do not refer to the release of calcium from the sarcoplasmic reticulum and it
speed of conduction of the action potential, but to the size is presumed that this occurs where the T-system and
of postsynaptic potential, and hence muscle twitch, that is sarcoplasmic reticulum form dyads. In the resting muscle,
produced. The difference probably resides in the amount the formation of cross-bridges between the actin and
of neurotransmitter released at the nerve/muscle junction myosin filaments is inhibited by a protein, tropomyosin,
following the arrival of the action potential (Usherwood, which blocks myosin binding sites on the actin molecules.
1974). Stimulation via the fast axon is presumed to release Tropomyosin is held by another protein, troponin, whose
a large amount of neurotransmitter and produces a large configuration is altered by binding with calcium so that
postsynaptic potential of consistent size followed by a tropomyosin no longer blocks the binding sites and myosin
brief, powerful contraction of the muscle (Fig. 10.16a). heads become linked to actin. Combination of ATP with
MUSCLE CONTRACTION 247
the myosin cross-bridges causes a conformational change 10.3.2.3 Inhibition of muscle contraction
and the link to actin is broken. In addition to the normal excitatory innervation, some
A cycle of muscle contraction and relaxation is associ- muscle fibers of some muscles are innervated by a neuron
ated with calcium release and then its sequestration. The that inhibits their activation. At an inhibitory
rapid removal of calcium from the system is associated nerve/muscle junction, a neural transmitter, probably ␥-
with the well-developed sarcoplasmic reticulum and, in aminobutyric acid (GABA), is released. It causes a change
general, twitch duration is inversely correlated with the in permeability at the postsynaptic membrane, but, unlike
quantity of sarcoplasmic reticulum present (Fig. 10.17a). the process occurring at an excitatory synapse, results in an
In asynchronous muscle the picture is different. An iso- influx of chloride ions. As a result, the membrane potential
lated muscle contracts in the same way as synchronous becomes even more negative, the membrane is hyperpolar-
muscle when stimulated at low frequencies and, at higher ized, and the tension exerted by the fiber decreases (Hoyle,
frequencies of stimulation, the muscle remains in a state of 1974; Usherwood, 1974).
sustained contraction (tetanus). However, this does not
happen in an oscillatory system, like the thorax, where the 10.3.2.4 Neuromodulation
muscles act antagonistically to each other. Here, the Many muscles, in addition to being innervated by excitatory,
muscles start to contract in response to a burst of action and perhaps also inhibitory neurons, receive input from
potentials, which presumably results in the release of neurons that release compounds modifying the muscle’s
calcium ions from the sarcoplasmic reticulum. However, response to normal excitation. Three chemicals have been
subsequent muscle oscillations are not related directly to commonly identified as such neuromodulators: octopamine,
nervous stimulation, hence the term asynchronous. 5-hydroxytryptamine (serotonin) and proctolin.
Further nervous stimulation is necessary only to maintain The octopamine-producing cells are situated in the
the level of muscle activity, perhaps by maintaining the level midline of a ganglion and are unpaired, their axons branch-
of calcium which remains in the sarcoplasm. The reduced ing to innervate muscles on either side of the body. Because
development of the sarcoplasmic reticulum appears to be of their positions they are called dorsal, unpaired, median
related to this failure to resequester calcium rapidly. cells (abbreviated to DUM) with a suffix to indicate the
Asynchronous muscles occur only in oscillating muscles that they innervate. Thus: DUMeti innervates the
systems such as the thorax where the contraction of one extensor tibiae muscle in the hind leg of a grasshopper;
flight muscle moves the wings and at the same time length- DUMdl innervates the dorsal longitudinal muscle; and
ens the antagonistic muscles. These sudden changes in DUMovi the muscles of the oviduct. Octopaminergic cells
length produce corresponding changes in muscle tension, are also known to supply the antennal muscles and, in
248 MUSCLES
Periplaneta, the muscles of the male accessory glands slow common fast
Dumeti excitor inhibitor excitor
(Allgäuer & Honegger, 1993; Sinakevitch et al., 1994). Not
all DUM cells are concerned with modulating muscular
activity and, in the desert locust, Schistocerca, only eight,
out of a total of 90 DUM cells in the metathoracic ganglion
are known to terminate at muscles.
The axons from DUM cells commonly accompany
1
motor axons to the muscles. Their terminal branches form octopamine
2
series of swellings, called varicosities which contain vesi-
cles varying in diameter from 60 to 230 nm and with an muscle fiber
electron dense core (unlike synaptic vesicles which are
electron lucent). They may, or may not contain
octopamine, but are clearly related to the secretion of the
compound (Hoyle, Colquhoun & Williams, 1980). Unlike
increased
the terminals of motor axons, there are no discrete twitch amplitude faster relaxation
nerve/muscle junctions and the axon terminals are separ-
ated from the muscle by thickened sarcolemma.
tension (mN)
Octopamine may have its effect both pre- and postsyn-
0.5
aptically (Fig. 10.19). It may cause more of the normal neu-
rotransmitter, L-glutamate, to be released, and it may elevate
the level of cAMP in the muscle (Whim & Evans, 1991). 0
These changes have been shown to have a variety of effects 0 100 200
time (ms)
on muscle activity. In the extensor tibiae muscle of
Stenopelmatidae (Orthoptera) it produces a sustained Fig. 10.19. Neuromodulation. Effect of octopamine on muscle
tension. Intrinsic rhythms in the same muscle in grass- activity. The effect may be presynaptic (1) or postsynaptic (2).
hoppers are eliminated by octopamine although its effects The latter increases the speed and amplitude of the twitch, the
are dependent on the level of activity of the slow axon to the former produces faster relaxation (after Evans, 1985).
muscles (Hoyle, 1985). In the dorsal longitudinal flight
muscles, octopamine increases the force generated when the muscles and some labral and antennal muscles.
muscle contracts and it also increases the rates of contraction Serotinergic neurons also run to the muscles of the fore-,
and relaxation. In locusts, octopamine does not induce these mid- and hindgut in the locust and cricket, and to the
changes after the teneral period (Whim & Evans, 1989). muscles of the reproductive system (Nässel, 1988).
Clearly, octopamine is likely to have a very important In Locusta, the serotinergic neurons of the mouthpart
role in modulating muscular activity during walking, muscles are known to be active during feeding, and the
jumping and flying, contributing to the behavioral versatil- serotonin they release is believed to modulate the activity
ity of insects. However, there is no certain information on of the muscles since, in vitro, it increases the amplitude and
its real role in the whole insect. (see Hoyle, 1985; Orchard, rate of contraction and the rate of relaxation (Baines,
Ramirez & Lange, 1993; Whim & Evans, 1989 for some Tyrer & Downer, 1990; Schachtner & Bräunig, 1993). Like
possible roles). octopamine, serotonin causes an increase in cAMP in the
Cells which produce serotonin and which have axons to muscle. Caterpillars do not have serotinergic neurons
the muscles of the mouthparts have been described in immediately associated with the muscles, but there may be
locust, a cricket and a cockroach. Periplaneta has two or a serotinergic neurohemal organ in the head which serves a
three pairs of such neurons in the subesophageal ganglion. similar function (Griss, 1990).
Their axons branch to form a fine network over the A peptide, proctolin, is present in some slow motor
surfaces of all the nerves to the mouthparts, forming a neurons, apparently being released at the same time as the
neurohemal organ (Davis, 1987). In Locusta the fibers principal neurotransmitter. It may act presynaptically, by
extend over the surface of the mandibular adductor increasing the rate at which the transmitter is released, and
ENERGETICS OF MUSCLE CONTRACTION 249
postsynaptically, enhancing the tension produced by generates a force as it contracts because of the resistance of
neural stimulation. It is known to be present in some axons the object being moved. The unit of force is called a
to the antennal muscles of Gryllus, Locusta and Periplaneta Newton (N). N ⫽kg m s⫺2.
and to an opener muscle of the ovipositor of Locusta. Tension is produced by opposing forces pulling on an
Neurons innervating a variety of visceral muscles in the object. Tension in a muscle normally rises to a peak as the
reproductive system and alimentary canal of Rhodnius are muscle begins to shorten and then falls again as shortening
also proctolinergic (Allgäuer & Honegger, 1993; Belanger continues. If there is no measurable change in length of the
& Orchard, 1993; Lange, 1993). muscle, it is said to be contracting isometrically. During
It is probable that modulation of muscle activity by isometric contraction, tension increases to a maximum. If
these and perhaps other compounds is a widespread and the muscle decreases in length, while tension remains con-
possibly universal phenomenon in insects. Even where stant, the contraction is said to be isotonic.
the muscles do not receive a direct neural supply of the Work is the application of a force over a distance, or a
compounds, it is likely that they are affected by their pres- measure of the energy transferred by a force.
ence in the hemolymph. Energy is the ability to do work. The unit of energy is
Review: Rheuben, 1995 the same as the unit of work, the joule (J). J ⫽kg m2 s⫺2.
Power is the rate of doing work, or the rate at which
10.3.2.5 Control of visceral muscles energy is supplied. The unit of power is the watt (W).
In innervated visceral muscles, the principles of muscle W ⫽kg m2 s⫺3
control are the same as in skeletal muscles. L-glutamate
may be involved as a neurotransmitter, but it is conceivable 10.4.2 Tension and force
that different transmitters are involved in different The tension exerted by insect muscles is not exceptional.
muscles (Usherwood, 1974). For instance, the mandibular muscles of various insects
In some insects, the heart is not innervated and the exert tensions of 3.6–6.9 g cm2, and the extensor tibiae
contractions of its muscles are myogenic. This does not muscle of Decticus (Orthoptera) 5–9 g cm2 compared with
mean that they are uncontrolled, and, for example, in the values of 6–10 g cm2 in humans.
Manduca it is known that heart muscle activity is modu- Because a muscle has intrinsic elasticity, tension does
lated by a neurosecretion from the corpora cardiaca. It is not fall to zero in the absence of stimulation. Some of this
probable that the activity of all non-innervated muscles is elasticity is attributed to the muscle attachments to the
controlled by blood-borne factors. cuticle and some to the sarcolemma, but the greater part
Myogenic contractions are commonly slow and rhyth- is due to elastic elements in the contractile system itself.
mic, but fast myogenic contractions also occur in some Energy is stored in this elastic system when the muscle is
muscles at some times. These are produced by action stretched. Flight muscles, and especially fibrillar
potentials generated spontaneously within some muscle muscles, have a much higher elasticity than other
fibers. Not all the fibers in a muscle appear able to produce muscles.
these action potentials and electrical activity spreads from The force exerted by a muscle is proportional to its
cell to cell, decreasing as the distance from the active cell cross-sectional area and, in general, this is not very great in
increases (Kalogianni & Theophilidis, 1995). insects. In some muscles, however, such as the extensor
Some muscles exhibit both neurogenic and myogenic tibiae of a locust, a considerable cross-sectional area is
contractions. This is the situation in muscles associated achieved by an oblique insertion of the muscle fibers into a
with the oviducts of orthopterans. large apodeme (see Fig. 10.4). As a result, this muscle can
exert a force of up to 15 N.
10.4 ENERGETICS OF MUSCLE
CONTRACTION 10.4.3 Twitch duration
The duration of each muscle twitch, the time for it to
10.4.1 Definitions shorten and relax, is dependent on temperature (Fig.
Force is an influence causing a mass to change its state of 10.17b). This is of critical importance in flight because
motion, so that it accelerates or decelerates. A muscle twitch duration limits the rate at which antagonistic
250 MUSCLES
expenditure of energy
Schistocerca requires a wingbeat frequency of about
20 Hz, with a period of about 50 ms. Only above 30 °C is 0
twitch duration short enough to avoid significant overlap
of antagonistic muscle twitches (Fig. 10.17b) and it is +ve
inertial force
therefore not surprising that sustained flight only occurs starting
at relatively high temperatures. 0
braking
Twitch duration also varies in different fiber types,
being shorter in fast than slow fibers. Fast fibers (short -ve
twitch) have fibrils that are small in cross-sectional area
with a relatively large proportion of sarcoplasmic reticu- Fig. 10.20. The forces involved in moving a wing. At the start of
lum. These factors are related to the readiness with which the stroke, most energy is used overcoming the inertia of the
wing. In midstroke, useful aerodynamic forces are produced. At
calcium reaches the most distant myofilaments and is rese-
the end of the stroke, the wing has considerable inertia (after
questered (see above). Twitch duration is not correlated
Alexander, 1995).
with fiber diameter, with sarcomere length or with the
volume of the fiber occupied by mitochondria (Josephson
& Young, 1987; Müller et al., 1992). energy then contributes to the beginning of the next half
stroke.
10.4.4 Power output Maximum efficiency is achieved only under certain
A muscle’s mechanical efficiency is defined as the ratio of conditions. Work output per cycle of contraction and
mechanical power output to metabolic energy consump- relaxation rises to a maximum and then declines as the fre-
tion. Direct measurements of the mechanical power quency of cycling increases. For the flight muscle of
output of flight muscles of Manduca and Bombus (insects Manduca at 35 °C, maximum efficiency occurs at a cycle
with synchronous and asynchronous flight muscles, frequency of about 30 Hz. Work per cycle, at the optimal
respectively) give maximum values of 130 and cycle frequency, increases with temperature, at least up to
110 W kg⫺1, respectively (Gilmour & Ellington, 1993; 40 °C.
Stevenson & Josephson, 1990). These values indicate The power output of a muscle may be increased by
mechanical efficiencies of 10% or less. Not all this power multiple stimulation via the motor axon, and such double
is available for mechanically useful work. In a flying insect, (or multiple) firing is commonly recorded when insects
energy is required not only to move the wing to produce appear to produce more power. This occurs, for instance,
aerodynamic force, but also to start it moving from an in the double firing of the axon to the second basalar
extreme, up or down, position, and for braking at the end muscle of Schistocerca (see Fig. 9.32), which may result in
of a half stroke (Fig. 10.20). The wing’s inertia towards the muscle more than doubling the amount of work which
the end of the half stroke stretches the antagonistic it does. The extra force exerted varies with the timing of
muscles, and this energy may be stored in elastic elements the second impulse relative to the first. In the basalar
within the muscle. As flight muscles only shorten by very muscle at 40 °C, the force is maximal when the second
small amounts, approximately 2% of their length, it is stimulus follows about 8 ms after the first. In the tettigo-
possible that the cross-bridges between thick and thin niid, Neoconocephalus, maximum power output from a ter-
filaments remain attached throughout the cycle of elonga- gocoxal muscle is achieved when the motor neuron fires
tion and contraction and function as springs (Alexander, three times with intervals of 4 ms between spikes
1995; Dickinson & Lighton, 1995). Energy may also be (Josephson, 1985). Multiple firing does not increase the
stored in elastic elements of the wing hinge as this is power output of all muscles at their normal operating fre-
stretched towards the end of the half stroke. This stored quencies, however (Stevenson & Josephson, 1990).
MUSCULAR CONTROL IN THE INTACT INSECT 251
a) synchronous muscle flight possible: (i) the loading of the muscle, (ii) the tem-
perature of the muscle, and (iii) the very slight contraction
neural
stimuli necessary to move the wing.
A maximum rate of shortening is achieved if the
muscle
contractions tension and loading of the muscle are maximal at the
beginning of contraction. Loading of flight muscles
involves the inertia of the wings, mechanical leverage of
neural
stimuli the wings, which changes in the course of a stroke,
damping of the movement of the wings by the air, and
muscle
contractions elastic loading due to the straining of the thorax and
stretching the antagonistic muscles. Inertia is highest at
the beginning of the stroke when the wing may be momen-
b) asynchronous muscle tarily stationary, or even moving in the opposite direction
(Fig. 10.20). Mechanical leverage of the wings and loading
neural due to the elasticity of the thorax are also greatest at this
stimuli
time and so will favor a high rate of shortening.
muscle The importance of temperature in governing the dura-
contractions
tion of the muscle twitch is considered in section 10.4.3.
Flight can only occur when muscle temperature is high
neural
stimuli enough to ensure rapid shortening and relaxation.
Finally, the wings are articulated with the thorax in
muscle such a way that only a very small contraction of the
contractions
muscles is necessary to produce a large movement of the
Fig. 10.22. Contraction of antagonistic muscle pairs (as in flight
wing: the flight muscles of Sarcophaga, for instance, only
muscles) in relation to neural stimulation. (a) Synchronous shorten by 1 or 2%, in the course of a wingstroke. As a
muscle. Each contraction results from the arrival of an action result the muscle twitch is brief despite the low rate of
potential. The stimuli to antagonistic muscles are in antiphase. shortening.
(b) Asynchronous muscle. Muscle oscillations occur In insects with synchronous flight muscles, each
independently of the arrival of action potentials which serve only contraction of the flight muscles is produced by the arrival
to keep the muscle in an activated state. The rate of neural input of a nerve impulse and the motor neurons to the antagonis-
to the antagonistic muscles may differ, as in this example. tic muscles fire approximately in antiphase (Fig. 10.22a).
These muscles occur in Odonata and orthopteroid insects
antagonist; it is stretched when the tymbal buckles out- as well as in Neuroptera, Trichoptera and Lepidoptera
wards (section 26.1.3). amongst the holometabolous insects. Wingbeat frequen-
When antagonistic muscles oscillate, they are driven by cies are generally less than 50 Hz although in some
motor neurons firing in antiphase (except for asynchro- Lepidoptera the frequency approaches 100 Hz.
nous flight muscles, see below). The precise timing of These muscles are generally activated by one or two
neural activity and the interplay of fast and slow excitatory action potentials in the motor axons, but in some
neurons and inhibitory neurons permits a wide range of Lepidoptera with very low wingbeat frequencies (5–10 Hz)
modulation. Section 8.4.1.4 describes neural regulation in the motor burst is characteristically 3–7 action potentials.
walking insects. The occurrence of two or more action potentials is associ-
The high wingbeat frequencies necessary for flight are ated with high lift requirements by the insects and results
produced by the rapid oscillation of pairs of antagonistic in higher power output by the muscles. Where longer
muscles. This is achieved despite the relatively low rate of bursts occur, the longer period of excitation keeps the
shortening of about 40 mm s⫺1 in Schistocerca and only muscles contracting for relatively long periods, and burst
11 mm s⫺1 in Sarcophaga. Three factors combine to length is inversely proportional to wingbeat frequency.
reduce the duration of the muscle twitch and so to make Manoeuvers in flight are achieved by alterations in the
REFERENCES 253
power output of specific muscles and by changes in the normally consists of a single spike; double firing does not
times at which different direct muscles, which affect wing usually occur. The frequency of the single spikes varies
twisting, are activated relative to each other. Figure 9.32 from 5 to about 25 Hz in different insects while wingbeat
illustrates some aspects of muscle coordination in flight. frequency varies from about 50 to over 200 Hz. The ratio
In insects with asynchronous muscles, the wingbeat of action potentials to wing cycles varies from about 1 : 5 to
frequency is often in excess of 100 Hz and it is a character- 1 : 40, but the rate of firing to antagonistic muscles is not
istic of these muscles that several contractions follow the necessarily the same. For example, during flight in the
arrival of each nerve impulse (Fig. 10.22b). Wingbeat fre- honeybee the dorsal longitudinal muscles are stimulated at
quency in these insects is determined primarily by the a lower frequency (about 86%) than the dorsoventral
mechanical properties of the thorax and the muscles muscles (Esch & Goller, 1991). Nevertheless, an increase
themselves. Neural inputs serve to maintain the muscles in the firing rate of the motor neurons does sometimes cor-
in an active state (see section 10.3.2.2). relate with an increase in wingbeat frequency.
Each neural signal to an asynchronous muscle Review: Kammer, 1985
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Growth and development of flight 85–113. Oxford: Pergamon Press. Functional aspects of the organisation
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Morgan, C.R. & Stokes, D.R. (1979). York: Academic Press. (1990). Effects of operating frequency
Ultrastructural heterogeneity of the Ready, N.E. & Josephson, R.K. (1982). and temperature on mechanical power
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PART III
The insect abdomen is more obviously segmental in origin stage larva hatches with only eight abdominal segments
than either the head or the thorax, consisting of a series of plus the telson; the remaining three segments are added at
similar segments, but with the posterior segments subsequent molts, arising behind the last abdominal
modified for mating and oviposition. In general, the segment, but in front of the telson. This type of develop-
abdominal segments of adult insects are without append- ment is called anamorphic.
ages except for those concerned with reproduction and a In general, the abdomen is clearly marked off from the
pair of terminal, usually sensory, cerci. Pregenital append- thorax, but this is not the case in Hymenoptera where the
ages are, however, present in Apterygota and in many first abdominal segment is intimately fused with the tho-
larval insects as well as in non-insectan hexapods. Aquatic racic segments and is known as the propodeum. The waist
larvae often have segmental gills, while many of Hymenoptera Apocrita is thus not between the thorax
holometabolous larvae, especially amongst the Diptera and abdomen, but between the first abdominal segment and
and Lepidoptera, have lobe-like abdominal legs called the rest of the abdomen. Often segment 2 forms a narrow
prolegs. petiole connecting the two parts. The swollen part of the
Reviews: Bitsch, 1979; Matsuda, 1976; Snodgrass, 1935 abdomen behind the waist is called the gaster (Fig. 11.2).
[259]
260 ABDOMEN
a) grasshopper
tergum tergum tergum tergum
tergum 2 tergum 4 6 8
1 3 tergum
5 tergum tergum
antecostal 7 tergum
sulcus 9
10 epiproct
(segment 11)
metapostnotum
paraproct
tympanum ovipositor
valves
spiracle 1 sternum sternum
sternum sternum 6 8
4 sternum sternum
sternum sternum 3
5 7
1 2
b) fly
tergum
tergum 4 tergum
3 5
tergum
2 intersegmental
membrane
tergum
6 tergum
7 tergum
8
tergum
spiracle 1 9
Fig. 11.1. Abdomen in lateral view. (a) An insect in which parts of all 11 segments are present in the adult (female red locust,
Nomadacris (Orthoptera)) (after Albrecht, 1956). (b) An insect with a reduced number of segments in the adult. Segments
6–9, which form the ovipositor, are normally retracted within the anterior segments (female housefly, Musca (Diptera) (after
Hewitt, 1914).
The more anterior segments have a spiracle on either posterior abdominal segments, or it may involve modified
side. This may be set in the pleural membrane (Fig. 11.3), abdominal appendages.
or in a small sclerite within the membrane, or on the side of In front of these genital segments the abdominal seg-
the tergum (Fig. 11.1) or sternum. The reproductive ments are usually unmodified, although segment 1 is fre-
opening in male insects is usually on segment 9, while in quently reduced or absent. Behind the genital segments,
the majority of female insects the opening of the oviduct is segment 10 is usually developed, but segment 11 is often
on or behind segment 8 or 9. The Ephemeroptera and represented only by a dorsal lobe, the epiproct, and two
Dermaptera are unusual in having the opening behind lateroventral lobes, the paraprocts. In Plecoptera,
segment 7. These genital segments may be highly Blattodea and Isoptera the epiproct is reduced and fused
modified, in the male to produce copulatory apparatus and with the tergum of segment 10, while in most
in the females of some orders to form an ovipositor. This holometabolous insects segment 11 is lacking altogether
may be formed by the sclerotization and telescoping of the and segment 10 is terminal.
ABDOMINAL APPENDAGES AND OUTGROWTHS 261
tergum
mesoscutum 6
pronotum tergum
7
propleuron sternum
sternum sternum sternum 7
leg 1 leg 2 leg 3 2 4 6
mesepisternum metapleuron sternum sternum
3 5
prolegs of caterpillars are homologous with the thoracic Apterygota and some related non-insect hexapods. On
legs (Panganiban, Nagy & Carroll, 1994). Some other abdominal segments 2–9 of Machilidae, 7–9 or 8–9 of
appendages are probably secondary structures which have Lepismatidae, 1–7 of Japygidae and 2–7 of Campodeidae
developed quite independently of the primitive append- there are pairs of small, unjointed styli, each inserted on a
ages. basal sclerite which is believed to represent the coxa (Fig.
The structure and functioning of the male and female 11.5a). Since similar styli are present on the coxae of the
genitalia are considered in chapters 12 and 13. Apart from thoracic legs of Machilis (Archaeognatha) these styli are
the genitalia and the cerci, abdominal appendages or other regarded as coxal epipodites.
outgrowths of the body wall tend to occur in larvae rather Associated with the styli, but occupying a more median
than in adults. The appendages of Apterygota and other position, are eversible vesicles. These are present on seg-
primitive hexapods are present in all stages of develop- ments 1–7 of Machilidae and 2–7 of Campodea (Diplura),
ment, however. but in Lepismatidae and Japygidae there are generally
fewer or none. The vesicles evert through a cleft at the
11.2.1 Abdominal appendages of primitive hexapods posterior margin of the segment, being forced out by
Styliform appendages Styliform structures, often associ- blood pressure (Fig. 11.5c,d). The retractor muscles of the
ated with eversible vesicles, are present on the abdomen of vesicles arise close together on the anterior margin of the
ABDOMINAL APPENDAGES AND OUTGROWTHS 263
vesicle retractor
muscle
sternum of next
segment
vesicle
intersegmental
membrane
sternum
sternum. Like those on the ventral tube of Collembola, vesicles. The vesicles are everted by blood pressure
these vesicles can absorb water from the substratum from within the body and are withdrawn by retractor
(Drummond, 1953). muscles.
There are pairs of appendages on each of the first three The ventral tube appears to have two functions. In
segments of the abdomen of Protura. At their most fully some circumstances it functions as an adhesive organ
developed they are two-segmented with an eversible enabling the insect to walk over smooth or steep surfaces.
vesicle at the tip (Fig. 11.5b). The appendages are moved To facilitate this on a dry surface the vesicles are moistened
by extrinsic and intrinsic muscles, which include a retrac- by a secretion from cephalic glands opening on to the
tor muscle of the vesicle. labium and connecting with the ventral tube by a groove in
the cuticle in the ventral midline of the thorax. The ventral
Abdominal appendages of Collembola The Collembola tube also enables Collembola to adhere to the surface film
have pregenital appendages on three abdominal seg- on water since it is the only part of the cuticle which is wet-
ments (see Fig. 8.25d). From the first segment a median table; all the rest is strongly hydrofuge.
lobe projects forwards and down between the last pair of The second function of the vesicles of the ventral tube
legs. This is known as the ventral tube and at its tip are a is the absorption of water from the substratum (section
pair of eversible vesicles which in many Symphypleona 18.4.1.2).
are long and tubular. The unpaired basal part of the The appendages of the third and fourth segments of the
ventral tube is believed to represent the fused coxae of abdomen of many Collembola form the retinaculum and
the segmental appendages and the vesicles are thus coxal the furca, which are used in locomotion (section 8.4.2.2).
264 ABDOMEN
a) simple
Fig. 11.7. Different types of cerci .
(a) Simple cercus [lateral view of tip
b) segmented
tergum epiproct of abdomen of male red locust,
tergum 10 tergum 7
cercus
Nomadacris (Orthoptera)]. (b)
9
tergum 9 Segmented [dorsal view of the tip
paraproct
cercus of the abdomen of male Periplaneta
tergum 10 (Blattodea)]. (c) Asymmetrical
(supra-anal plate)
[ventral view of tip of abdomen of
stylus male Idioembia (Embioptera)]. (d)
sternum 9 Sexually dimorphic [male and female
(subgenital plate)
forceps (cerci) Forficula
sternum
8 (Dermaptera)].
right left
cercus cercus
cercus
cercus
sclerotized walls and an extensively folded roof (Fig. 11.6b). segmented as in Blattodea and Mantodea (Fig. 11.7b). They
Muscles inserted into the roof and the rim of the sclerotized may be very short and barely visible or long and filamentous,
walls of the inner chamber increase the volume of the as long or longer than the body as in Thysanura,
chamber when they contract and if at the same time the rim Ephemeroptera and Plecoptera. Even within a group, such
of the sucker is pressed down on to the substratum a partial as the Acridoidea, the range of form of the cerci is consider-
vacuum is created so that the sucker adheres to the surface. able (Uvarov, 1966). In cockroaches, where the cerci are seg-
Even if a well-formed sucker is not present, many mented, additional segments are added at each molt. The
dipterous larvae can produce a sucker-like effect by raising first instar cercus of Periplaneta has three segments, while in
the central part of the ventral surface while keeping the the adult male it has 18 or 19 and in the adult female 13 or 14.
periphery in contact with the substratum, the sucker being Growth results from division of the basal segment.
sealed and made effective by a film of moisture. The cerci are usually set with large numbers of trichoid
sensilla. Sometimes these sensilla are filiform and are sen-
11.2.3 Sensory structures sitive to air movements. This is true in cockroaches and
Most insects have mechanosensitive sensilla on the crickets where different filiform hairs are maximally sensi-
abdominal segments, and grasshoppers also have small tive to air movements from different directions (section
contact chemoreceptors scattered amongst the 23.1.3.1). In the female of the sheep blowfly, Lucilia, there
mechanoreceptors (Thomas, 1965). In addition, the are also a small number of contact chemoreceptors and
appendages of segment 11 often form a pair of structures olfactory receptors on the cerci (Merritt & Rice, 1984).
called cerci which usually function as sense organs. This may also be true in other insects.
Cerci are present and well-developed in the Apterygota Sometimes the cerci differ in the two sexes of a species,
and the hemimetabolous orders other than the hemipter- and they may play a role in copulation. Thus the cerci of
oids. In holometabolous insects, cerci are present in the female Calliptamus (Orthoptera) are simple cones, but in the
adults of Mecoptera and some Diptera; they are not present male they are elongate, flattened structures with two or three
in holometabolous larvae. The cerci may be simple, unseg- lobes at the apex armed with strong inwardly directed points.
mented structures as in Orthoptera (Fig. 11.7a), or multi- There is similar dimorphism in Embioptera, where the male
266 ABDOMEN
urogomphus
segment 10
cerci are generally asymmetrical with the basal segment of the called gills, surrounding the anus. They are concerned
left cercus forming a clasping organ (Fig. 11.7c), and amongst with salt regulation (section 18.3.2.2) and are found in
the earwigs the cerci form powerful forceps which are usually larval mosquitoes and chironomids, where a group of four
straight and unarmed in the female, but incurved and toothed papillae surrounds the anus (see Fig. 18.3), and in some
in the male (Fig. 11.7d). Similar forceps-like cerci in the larval Trichoptera.
Japygidae are used in catching prey. In some holometabolous
insects they form part of the external genitalia. 11.2.5 Secretory structures
The cerci of larval Zygoptera are modified to form the Some insects have glands opening on the abdomen which
two lateral gills (see Fig. 17.28), while in the probably have a defensive function in most cases (see
ephemeropteran Prosopistoma the long, feather-like cerci, Chapter 27). Most aphids have a pair of tubes, known as
together with the median caudal filament, can be used to siphunculi, or cornicles, projecting from the dorsum of
drive the insect forwards by beating against the water. segment 5 or 6, or from between them. Each cornicle has a
terminal opening which is normally closed by a flap of
11.2.4 Gills cuticle controlled by an opener muscle and the whole
Gills are present on the abdominal segments of the larvae structure can be moved by a muscle inserted at the base so
of many aquatic insects. Ephemeroptera usually have six or that the cornicle can be pointed in various directions, even
seven pairs of plate-like or filamentous gills (see Figs. 15.4, forwards. Aphids release an alarm pheromone from the
18.2) which are moved by muscles. They may play a direct cornicles if they are attacked by parasites or predators
role in gaseous exchange, but perhaps are more important (section 27.1.6.1). This causes a response in other aphids
in maintaining a flow of water over the body. Gill tufts may of the same species, but the response differs in different
also be present on the first two or three abdominal seg- species. Individuals of Schizaphis graminum usually drop
ments, or in the anal region of larval Plecoptera. The larva off the plant when they perceive the pheromone; Myzus
of Sialis (Megaloptera) has seven pairs of five-segmented persicae may drop off the plant, or walk away from the
gills, each arising from a basal sclerite on the side of the feeding site; other species jerk about in a manner which is
abdomen (Fig. 11.8a), and a terminal filament of similar presumed to discourage attack without withdrawing their
form arises from segment 9. Similar, but unsegmented stylets from the host. The effective radius of the
gills are present in other larval Megaloptera and in some pheromone may extend up to about 3 cm from the emitting
larval Coleoptera. Larval Trichoptera have filamentous aphid (Nault & Phelan, 1984).
gills in dorsal, lateral and ventral series. The first abdominal appendages are well developed in
Some aquatic larvae have papillae, often incorrectly the embryos of insects belonging to a number of groups.
REFERENCES 267
They are known as pleuropodia (section 14.2.10), but they Caterpillars of some families have branched projec-
do not persist after hatching. Perhaps their primary func- tions of the body wall on some or all of the body segments,
tion is the secretion of enzymes which digest the serosal both thorax and abdomen. These projections are called
cuticle prior to hatching. scoli and possibly have defensive functions. Similar struc-
tures are found on some larval Mecoptera and Coleoptera
11.2.6 Other abdominal structures (Stehr, 1987).
Apart from the segmentally arranged prolegs and gills Sometimes the prolegs are modified for functions other
some insects have other abdominal appendages which than walking. In some Notodontidae the anal prolegs are
often appear to have a defensive role, but whose function is modified for defensive purposes. Thus in the larva of the
sometimes unknown. Some groups of insects have a puss moth, Cerura, they are slender projections which nor-
median process projecting from the last segment. In mally point posteriorly, but, if the larva is touched, the tip of
Thysanura and Ephemeroptera this is in the form of a the abdomen is flexed forwards and a slender pink process is
median caudal filament which resembles the two cerci everted from the end of each projection. At the same time
(Fig. 11.8d). Larval Zygoptera have a median terminal gill the larva raises its head and thorax from the ground and
on the epiproct, while in larval hawkmoths (Sphingidae) a emits formic acid from a ventral gland in the prothorax.
terminal spine arises from the dorsum of segment 10. This reaction is presumed to be a defensive display.
Some larval Coleoptera have a pair of processes called In a few larval Diptera, prolegs may be used for holding
urogomphi, which are outgrowths of the tergum of prey. The larva of Vermileo lives in a pit in dry soil and
segment 9 (Fig. 11.8c). They may be short spines or multi- feeds in the same way as an antlion. It lies ventral side up,
articulate filaments and they may be rigid with the tergum and prey which fall into the pit are grasped against the
or arise from the membrane behind it so that they are thorax by a median proleg on the ventral surface of the first
mobile. Jeannel (1949) regards them as homologous with abdominal segment.
cerci, but see Crowson (1960).
REFERENCES
Albrecht, F. O. (1956). The anatomy of Hinton, H. E. (1955). On the structure, Panganiban, G., Nagy, L. & Carroll, S.B.
the red locust, Nomadacris septemfasci- function, and distribution of the (1994). The role of the distal-less gene
ata Serville. Anti-Locust Bulletin no. 23, prolegs of the Panorpoidea, with a crit- in the development and evolution of
9 pp. icism of the Berlese–Imms theory. insect limbs. Current Biology, 4, 671–5.
Bitsch, J. (1979). Morphologie abdomi- Transactions of the Royal Entomological Snodgrass, R. E. (1935). Principles of
nale des insectes. In Traité de Zoologie, Society of London, 106, 455–545. Insect Morphology. New York:
vol. 8, part 2, ed. P.-P.Grassé, pp. Jeannel, R. (1949). Ordre des McGraw-Hill.
291–587. Paris: Masson et Cie. Coléoptéroïdes. In Traité de Zoologie, Snodgrass, R. E. (1956). Anatomy of the
Crowson, R. A. (1960). The phylogeny of vol. 9, ed. P.-P.Grassé, pp. 771–891. Honey Bee. London: Constable.
Coleoptera. Annual Review of Paris: Masson et Cie. Stehr, F. W. (ed.) (1987) Immature Insects,
Entomology, 5, 111–34. Matsuda, R. (1976). Morphology and vol. 1. Dubuque, Iowa: Kendall/Hunt
Drummond, F. H. (1953). The eversible Evolution of the Insect Abdomen. Publishing Co.
vesicles of Campodea (Thysanura). Oxford: Pergamon Press. Thomas, J.G. (1965) The abdomen of the
Proceedings of the Royal Entomological Merritt, D.J. & Rice, M.J. (1984) female desert locust (Schistocerca gre-
Society of London A, 28, 115–8. Innervation of the cercal sensilla on the garia Forskål) with special reference to
Hewitt, C. G. (1914). The House-Fly, ovipositor of the Australian sheep the sense organs. Anti-Locust Bulletin
Musca domestica Linn. Cambridge: blowfly (Lucilia cuprina). Physiological no. 42, 20pp.
Cambridge University Press. Entomology, 9, 39–47. Uvarov, B. P. (1966). Grasshoppers and
Nault, L.R. & Phelan, P.L. (1984). Alarm Locusts, vol. 1. Cambridge: Cambridge
pheromones and presociality in pre- University Press.
social insects. In Chemical Ecology of
Insects. ed. W.J. Bell & R.T. Cardé, pp.
237–56. New York: Chapman & Hall.
12 Reproductive system: male
12.1 ANATOMY OF THE INTERNAL At least some of the cells of the vas deferens are glandular,
REPRODUCTIVE ORGANS secreting their products into the lumen (Riemann &
Giebultowicz, 1991).
The male reproductive organs typically consist of a pair of
The seminal vesicles, in which sperm are stored before
testes connecting with paired seminal vesicles and a
transfer to the female, are dilations of the vasa deferentia in
median ejaculatory duct (Fig. 12.1). In most insects there
many insects (Fig. 12.1b), but in some Hymenoptera and
are also a number of accessory glands which open into the
nematoceran Diptera they are dilations of the ejaculatory
vasa deferentia or the ejaculatory duct.
duct. Lepidoptera have both structures: sperm are stored
Testis The testes may lie above or below the gut in the temporarily in expanded regions of the vasa deferentia and
abdomen and are often close to the midline. Usually each then are transferred to dilations in the upper part of the
testis consists of a series of testis tubes or follicles ranging ejaculatory duct, known as the duplex (Fig. 12.14). In
in number from one in Coleoptera Adephaga to over 100 in Orthopteroidea and some Odonata, Phthiraptera and
grasshoppers (Acrididae). Sometimes, as in Lepidoptera, Coleoptera, they are not simply expansions of the male
the follicles are incompletely separated from each other ducts, but are separate structures (Fig. 12.1a). In some
(Fig. 12.2c), and the testes of Diptera consist of simple, insects, the seminal vesicles are epidermal in origin and in
undivided sacs, which may be regarded as single follicles. these cases they are lined with cuticle.
Sometimes the follicles are grouped together into several The cellular lining of the seminal vesicles is glandular
separate lobes (Fig. 12.1b). In the cerambycid, Prionoplus, and probably provides nutrients for the sperm.
for example, each testis comprises 12 to 15 lobes each with
15 follicles. The testes of Apterygota are often undivided Ejaculatory duct The vasa deferentia join a median duct,
sacs, but it is not certain in this case that they are strictly called the ejaculatory duct, which usually opens posteri-
comparable with the gonads of other insects since the orly in the membrane between the ninth and tenth abdom-
germarium occupies a lateral position in the testis instead inal segments (gonopore in Fig. 12.7). Ephemeroptera
of being terminal. have no ejaculatory duct and the vasa deferentia lead
The wall of a follicle is a thin epithelium, sometimes directly to the paired genital openings. Dermaptera, on the
consisting of two layers of cells, standing on a basal lamina. other hand, have paired ejaculatory ducts, although, in
The follicles are bound together by a peritoneal sheath and some species, one of the ducts remains vestigial. Thus in
if the two testes are close to each other they may be bound Forficula the righthand ejaculatory duct is fully functional
together. In some Lepidoptera, the two testes fuse com- while the lefthand duct is vestigial (Popham, 1965).
pletely to form a single median structure. The epithelium of the ejaculatory duct is one cell thick
and, as it is epidermal in origin, it is lined with cuticle.
Vas deferens and seminal vesicle From each testis follicle, a Often at least a part of the wall is muscular, although the
fine, usually short, vas efferens connects with the vas defer- ejaculatory duct in Apis is entirely without muscles. Parts
ens (plural: vasa deferentia) (Fig. 12.2b), which is a tube with of the wall of the duct may be glandular, contributing to
a fairly thick bounding epithelium, a basal lamina and a layer the formation of the spermatophore.
of circular muscle outside it. The vasa deferentia run back- Where a complex spermatophore is produced, the
wards to lead into the distal end of the ejaculatory duct1. ejaculatory duct is also complex. Thus in Locusta
1 Note: distal and proximal are used throughout this text with refer-
(Orthoptera), the ejaculatory duct consists of upper and
lower ducts connected via a funnel-like constriction (Fig.
ence to the origin of any structure. The ejaculatory duct originates
as an invagination of the ectoderm. Thus, the part nearest the body 12.13). The upper part of the duct into which the acces-
wall at the point of origin is proximal; the part most remote from sory glands open has a columnar epithelium and thin
the body wall is distal. cuticle and the lumen is a vertical slit in cross section. In
[268]
ANATOMY OF THE INTERNAL REPRODUCTIVE ORGANS 269
a) Locusta
bean-shaped
tubular gland gland
seminal vesicle
vas deferens
lobe of
testis
vas deferens
accessory glands
(unravelled) accessory glands
(normal position)
seminal
vesicle ejaculatory duct
ejaculatory duct
Fig. 12.1. Basic structure of the internal reproductive organs of the male. (a) An insect with a large number of testis follicles
and accessory glands. The testes lie close together in the midline, but are distinct. The glands are of different types (but this is
not shown in the diagram) (Locusta, Orthoptera) (from Uvarov, 1966). (b) An insect with several distinct testis lobes and only
two pairs of accessory glands (Tenebrio, Coleoptera) (from Imms, 1957).
the funnel, the cuticle is thicker and forms nine (usually) produce a variety of secretions which contribute to the
ridges on either side. These curve upwards posteriorly as spermatophore. The constrictions make it possible for the
they run back to meet in the dorsal midline and they secretions of different sections to be used separately and in
project so that they almost completely divide the lumen. sequence (Lai-Fook, 1982a,b).
The lumen of the lower duct is circular in cross section
and leads to the ejaculatory sac and spermatophore sac. Accessory glands The male accessory glands may be ecto-
Scattered muscle fibers are present in the wall of the dermal or mesodermal in origin, when they are known as
upper duct but are absent elsewhere. The ejaculatory duct ectadenia or mesadenia, respectively. Ectadenia, which
of the milkweed bug, Oncopeltus, is also extremely open into the ejaculatory duct, occur in many Coleoptera,
complex, being specialized for erection of the penis (Fig. in the Diptera Nematocera and some Homoptera.
12.10). Mesadenia, which open into the vasa deferentia or the
The ejaculatory duct in Lepidoptera is extended distal end of the ejaculatory duct, are found in Orthoptera
inwards as an unpaired duct of mesodermal origin and so and many other orders. In some species of Heteroptera and
not lined with cuticle. This is called the simplex. It bifur- Coleoptera, both ectadenia and mesadenia are present.
cates distally to connect with the accessory glands and vasa The number and arrangement of accessory glands
deferentia and this part is known as the duplex (Fig. varies considerably between different groups of insects. In
12.14). The simplex produces most of the spermatophore Lepidoptera there is a single pair of glands (Fig. 12.14); in
since Lepidoptera have only a single pair of accessory Tenebrio, there are two pairs (Fig. 12.1b). In contrast,
glands. In Calpodes, it is divided into seven sections par- Schistocerca and Locusta have 15 pairs of accessory glands,
tially separated from each other by constrictions, and some not counting the seminal vesicles with which they are
of these are further differentiated into zones of cells with closely associated (Fig. 12.1a), and Gryllus has over 600.
different structures. These different sections and zones Sometimes there are no morphologically distinct accessory
270 REPRODUCTIVE SYSTEM: MALE
a) b) c)
follicle peritoneal sheath
gland
follicle follicle epithelium
vas efferens
vas deferens
opening to
ejaculatory
duct
Fig. 12.2. Male reproductive organs. (a) Accessory gland. Diagram of the bean-shaped gland of Tenebrio (see Fig. 12.1b)
showing that different regions contain cells producing different secretions (shown by different shading). Two additional cell
types also occur, but are not in the plane of this section (after Dailey, Gadzama & Happ, 1980). (b) Testis. Diagram of a series
of testis follicles opening independently into the vas deferens, as in Orthoptera. (c) Testis. Diagrammatic section through a
testis in which the follicles are incompletely separated from each other and have a common opening to the vas deferens, as in
Lepidoptera (from Snodgrass, 1935).
glands. This is the case in Apterygota, Ephemeroptera and proctolinergic DUM neurons (section 10.3.2.4) with cell
Odonata, and muscoid Diptera. bodies in the terminal abdominal ganglion. At least some
Each accessory gland consists of a single layer of epi- of the muscles are also innervated by other neurons which
thelial cells whose fine structure varies depending on their may be inhibitory (Kimura, Yasuyama & Yamaguchi,
stage of development and also on the nature of the secre- 1989). In Periplaneta, the DUM cells innervating the
tion produced. Where the glands are few in number, accessory glands are octopaminergic (Sinakevitch et al.,
different regions within them may be functionally dis- 1994).
tinguishable. In Tenebrio, for example, the tubular glands The accessory glands become functional in the adult
produce three classes of compounds, and the bean-shaped insect. Their secretions are involved in producing the
glands have eight morphologically distinguishable cell spermatophore, where one is present, and also in trans-
types secreting a number of different products (Fig. 12.2a). ferring to the female chemicals that modify her behavior
In Lepidoptera, the accessory glands are regionally and physiology (see below).
differentiated to produce two different secretions (Fig. Reviews: Chen, 1984 – structure and biochemistry; Gillott, 1988
12.14). On the other hand, where many glands are present, – general; Happ, 1984 – structure and development; Happ, 1992
several glands may produce the same proteins. This is the – structure and control of development; Snodgrass, 1935 –
case in the Orthoptera. In Schistocerca, seven of the 15 structure
pairs of glands appear to produce a single product, while
most of the other pairs each produce a unique product.
Where there are few or no accessory glands, their role is 12.2 SPERMATOZOA
sometimes taken over by glandular cells in the ejaculatory
duct. This is most obvious in the lepidopteran simplex, 12.2.1 Structure of mature spermatozoa
but also occurs in muscoid Diptera. The mature sperm of most insects are filamentous, often
Outside the epithelium is a muscle layer which, in about 300 m long and less than a micron in diameter with
Gryllus, consists of a single layer of fibers wound round the head and tail regions of approximately the same diameter
gland in a tight spiral, but with a more complex arrange- (Fig. 12.3) (but the sperm of some Drosophila (Diptera)
ment round the openings of the glands to the ejaculatory species may be 15 mm long). The sperm has a typical cell
duct. In this insect, both sets of muscles are innervated by membrane about 10 nm thick, coated on the outside by a
SPERMATOZOA 271
acrosome extra-acrosomal
nucleus layer
radial
axoneme accessory link
tubule coarse
fibers
central coarse
tubule mitochondrial
fibers derivative
central
tubule
outer mitochondrial
doublet derivative
cylinder
doublet
central
tubule
Fig. 12.3. Diagram showing the structure of a sperm in longitudinal section with representative cross-sections at the points
shown.
layer of glycoprotein known as the glycocalyx. In fleas this without nuclei (apyrene) so that they cannot effect
is about 13 nm thick, and in grasshoppers about 30 nm. fertilization of the egg. Spermatids which give rise to them
The glycocalyx is made up of rods at right angles to the have numerous micronuclei instead of a single nucleus and
surface of the sperm (Fig. 12.4a). Lepidopteran sperm these micronuclei subsequently break down completely.
have a series of projections called lacinate appendages Apyrene sperm are formed in separate cysts from the
running along their length. They are made up of thin eupyrene sperm.
laminae stacked parallel with, but external to, the surface In front of the nucleus is the acrosome. This is a mem-
membrane (Fig. 12.4b). These structures are no longer brane-bound structure of glycoprotein with, in most
present when the sperm are released from the cyst (section insects, a granular extra-acrosomal layer and an inner rod
12.2.4), but the material of which they are composed may or cone. Neuropteran sperm have no acrosome and occa-
subsequently be used in binding the sperm together. sional species with no acrosome occur in other orders. The
The greater part of the head region is occupied by the acrosome is probably involved with attachment of the
nucleus (Fig. 12.3). In mature sperm of most species, the sperm to the egg and possibly also with lysis of the egg
nucleus is homogeneous in appearance, but sometimes, as membrane, thus permitting sperm entry.
in the grasshopper Chortophaga, it has a honeycomb Immediately behind the nucleus, the axial filament, or
appearance. The DNA is apparently arranged in strands axoneme, arises. In most cases this consists of two central
parallel with the long axis of the sperm. In Lepidoptera, a tubules with a ring of nine doublets and nine accessory
second kind of sperm is produced in addition to the tubules on the outside (Figs. 12.3, 12.4). The central
normal nucleate (eupyrene) sperm. These sperm are tubules are surrounded by a sheath and are linked radially
272 REPRODUCTIVE SYSTEM: MALE
glycocalyx
cell
membrane
mitochondrial
derivative
100 nm
nucleus
cell
membrane
reticular
appendage
axial
filament
lacinate
appendage
100 nm
SPERMATOZOA 273
to the doublets. Additional fibers are usually present 12.2.2 Sperm bundles
between the accessory tubules. Some unusual exceptions In a number of insects, sperm are grouped together in
to this 9 ⫹9 ⫹2 arrangement occur. Accessory tubules are bundles which sometimes persist even after transfer to the
lacking in Collembola, Japygidae (Diplura), Mecoptera female. The sperm of Thermobia (Thysanura) normally
and Siphonaptera. occur in pairs, the two individuals being twisted round
The sperm of some insects have two axial filaments. each other with their membranes joined at points of
This occurs in Psocoptera, Phthiraptera, Thysanoptera contact (Dallai & Afzelius, 1984). Pairs of sperm also occur
and many bugs. In Sciara (Diptera), there is no well-orga- in some Coleoptera.
nized axial filament, but 70–90 tubule doublets, each with Coccids have much more specialized sperm bundles.
an associated accessory tubule, are arranged in a spiral In these insects, each cyst (see section 12.2.3) commonly
which encloses the mitochondrial derivative posteriorly. It produces 32 sperm which may become separated into two
is presumed that the axial filament or the equivalent struc- bundles of about 16. Some species have 64 sperm in a
ture causes the undulating movements of the tail which bundle. Each bundle becomes enclosed in a membranous
drive the sperm forwards. sheath and the cyst wall degenerates. The sheath of many
The sperm of Pterygota have two mitochondrial deriv- species, such as Pseudococcus, is longer than the sperm,
atives which flank the axial filament. Within these the which occupy only the middle region, and the head-end of
cristae become arranged as a series of lamellae projecting the sheath has a corkscrew-like form. The sperm bundles
inwards from one side of the derivative and at right angles of Parlatoria, on the other hand, are only the same length
to its long axis. The matrix of the derivative is occupied by as the sperm, which are all oriented in the same direction
a paracrystalline material. Sperm of Mecoptera and within the bundle. Movement of the bundles does not
Trichoptera and species of some other orders have only normally occur until they enter the female. It results from
one mitochondrial derivative, while phasmids have none at the combined activity of the sperm within. Subsequently,
all (but this does not mean that they are without respira- the sheath of the bundle ruptures and the sperm are
tory enzymes, see below). More or less normal mitochon- released.
dria persist in the sperm of Apterygota and non-insect In some Orthoptera and Odonata, different types of
Hexapoda except that they fuse together and become elon- sperm bundle, known as spermatodesms, are formed. The
gated. There are three such mitochondria in the sperm tail spermatodesms of tettigoniids comprise about ten sperm
of Collembola, and two in Diplura and Machilidae. anchored together by their acrosomes. These bundles are
Coccid sperm occur in bundles and lack all the typical released from the testis and the sperm heads then become
organelles. The nucleus is represented by an electron- enclosed in a muff of mucopolysaccharide secreted by the
opaque core with no limiting membrane. Mitochondrial gland cells of the vas deferens. In acridids, the sperma-
derivatives are absent, but the homogeneous cytoplasm of todesms are completely formed within the testis cyst and
the sperm probably contains the enzymes with a respira- may include all the sperm within the cyst. The sper-
tory function. Each sperm has 45–50 microtubules in a matids come to lie with their heads oriented towards a
spiral round a central mass of chromatin. They run the cyst cell and extracellular granular material round the
whole length of the sperm and may be concerned with its acrosome of each coalesces to form a cap in which the
motility, replacing the typical axial filament (Swiderski, heads of all the sperm are embedded. The spermatodesms
1980). of Acrididae persist until they are transferred to the
Sperm of Kalotermitidae and Rhinotermitidae have female.
no flagellum at all. The sperm of Reticulitermes
(Rhinotermitidae) is spherical with no acrosome, but it has 12.2.3 Spermatogenesis
a few normal mitochondria and two short axial filaments At the distal end of each testis follicle is the germarium, in
although these do not extend into a tail. It is presumed that which the germ cells divide to produce spermatogonia (cells
this sperm is non-motile. Non-motile sperm also occur in which divide mitotically to produce spermatocytes; sper-
the dipteran family Psychodidae and in Eosentomon matocytes divide meiotically to produce spermatids) (Fig.
(Protura). 12.5). In Orthoptera, Blattodea, Homoptera and Lepi-
Review: Jamieson, 1987 – structure and evolution doptera, the spermatogonia probably obtain nutriment
274 REPRODUCTIVE SYSTEM: MALE
apical cell
vas deferens cysts
Fig. 12.5. Diagram of a testis follicle showing the sequence of stages of development of the sperm (from Wigglesworth,
1965).
from a large apical cell with which they have cytoplasmic II:I a zone of maturation and reduction, in which each
connections, while in Diptera and Heteroptera an apical spermatocyte undergoes the two meiotic divisions to
syncytium performs a similar function. Transfer of mito- produce spermatids;
chondria from this syncytium to the spermatogonia has III: a zone of transformation, in which the spermatids
been observed in Diptera. develop into spermatozoa, a process known as
The apical connections are soon lost and the spermato- spermiogenesis.
gonia associate with other cells which form a cyst around
them (Fig. 12.5). One, or sometimes more, spermatogonia The number of sperm ultimately produced by a cyst
are enclosed in each cyst and, in Prionoplus, there are ini- depends on the number of spermatogonial divisions and
tially two cyst-cells round each spermatogonium. They this is fairly constant for a species. In grasshoppers
may supply nutriment to the developing sperm and, in (Acrididae), there are between five and eight spermatogo-
Popillia (Coleoptera), nutrient transfer may be facilitated nial divisions and Melanoplus, which typically has seven
by the sperm at one stage having their heads embedded in divisions before meiosis, usually has 512 sperm per cyst.
the cyst-cells. In Heteroptera, large cells with irregular Normally four spermatozoa are produced from each sper-
nuclei, called trophocytes, are scattered amongst the matocyte, but in many coccids the spermatids which
cysts. possess heterochromatic chromosomes degenerate so that
As more cysts are produced at the apex of a follicle, only two sperm are formed from each spermatocyte and 32
they displace those which have developed earlier so that a are present in each cyst. In Sciara (Diptera), only one sper-
range of developmental stages is present in each follicle matid is formed from each spermatocyte because of an
with the earliest stages distally in the germarium and the unequal distribution of chromosomes and cytoplasm at
oldest in the proximal part of the follicle adjacent to the vas the meiotic divisions.
deferens. Three zones of development are commonly rec- Review: Tuzet, 1977a
ognized below the germarium (Fig. 12.5):
12.2.3.1 Spermiogenesis
I: a zone of growth, in which the primary spermatogonia, The spermatid produced at meiosis is typically a rounded
enclosed in cysts, divide and increase in size to form cell containing normal cell organelles. It subsequently
spermatocytes; becomes modified to form the sperm and this process of
SPERMATOZOA 275
spermiogenesis entails a complete reorganization of the to form a pair of ribbon-like structures. At the same time,
cell. It is convenient to consider separately each organelle their internal structure is reorganized so that the cristae
of the mature sperm. form a series of parallel lamellae along one side and the
matrix is replaced by paracrystalline material.
Acrosome The acrosome is derived, at least in part, from
Golgi material, which in spermatocytes is scattered Centriole and axial filament Young spermatids contain
through the cytoplasm in the form of dictyosomes. There two centrioles oriented at right angles to each other and
may be 30 or 40 of these in the cell and they consist of each composed, as in most cells, of nine triplets of tubules.
several pairs of parallel membranes with characteristic One gives rise to the axial filament, but ultimately both
vacuoles and vesicles. After the second meiotic division the centrioles disappear. The tubules of the axial filament
dictyosomes in Acheta fuse to a single body called the grow out from the centriole and finally extend the length of
acroblast, which consists of 6–10 membranes forming a the sperm’s tail. The accessory tubules arise from tubule
cup with vacuoles and vesicles both inside and out. In the doublets, appearing first as side arms, which become C-
later spermatid, a granule, called the pro-acrosomal shaped and then separate off and close up to form cylin-
granule, appears in the cup of the acroblast and increases ders. The development of accessory tubules is discussed
in size. The acroblast migrates so that the open side faces by Dallai and Afzelius (1993).
the nucleus, and then the granule, associated with a newly
developed membrane, the interstitial membrane, moves 12.2.3.2 Biochemical changes
towards the nucleus and becomes attached to it. As the cell The repeated cell divisions during spermatogenesis entail
elongates, the acroblast membranes migrate to the poste- the synthesis of large amounts of DNA and RNA, but syn-
rior end of the spermatid and are sloughed off together thesis of DNA stops before meiosis occurs, while RNA
with much of the cytoplasm and various other cell inclu- synthesis continues into the early spermatid.
sions. The pro-acrosomal granule then forms the acro- Subsequently, no further synthesis occurs and RNA is
some, becoming cone-shaped and developing a cavity in eliminated first from the nucleus and then from the cell as
which an inner cone is formed. In Gelastocoris the nucleus elongates. The reduction in RNA synthesis is
(Heteroptera), the pro-acrosome is formed from the fusion associated with a rise in the production of an arginine-rich
of granules in the scattered Golgi apparatus and no acro- histone which forms a complex with DNA stopping it
blast is formed. This may also be the case in Acrididae. from acting as a primer for RNA synthesis, and, perhaps,
insulating the genetic material from enzymic attack during
Nucleus In the early spermatid of grasshoppers the transit to the egg.
nucleus appears to have a typical interphase structure with
the fibrils which constitute the basic morphological units 12.2.3.3 Control of spermatogenesis
of the chromosomes unoriented. As the sperm develops, The spermatocytes reach meiosis before the final molt in
the nucleus becomes very long and narrow and the most insect species and, in species which do not feed as
chromosome fibrils become aligned more or less parallel adults, the whole process of spermatogenesis may be com-
with its long axis. The nucleoplasm between the fibrils is plete before adult eclosion (Fig. 12.6). In many species,
progressively reduced until finally the whole of the however, spermatogenesis continues for an extended
nucleus appears to consist of a uniformly dense material. A period and new sperm continue to be produced through-
similar linear arrangement of the chromosomes occurs in out adult life. The time taken for the completion of
other groups. spermatogenesis varies, but in Melanoplus the spermato-
gonial divisions take eight or nine days and spermiogene-
Mitochondria In the spermatid, the mitochondria fuse to sis, ten. In the skipper butterfly, Calpodes, spermiogenesis
form a single large body, the nebenkern, consisting of an takes about four days (Lai-Fook, 1982c).
outer limiting membrane and a central pool of mitochon- The factors regulating spermatogenesis are not well
drial components. The nebenkern separates into two mito- understood. At least in Lepidoptera, ecdysteroids have
chondrial derivatives associated with the developing axial some role, but this differs from species to species.
filament immediately behind the nucleus. They elongate Spermatogenesis in the larva proceeds as far as prophase of
276 REPRODUCTIVE SYSTEM: MALE
endophallus
ejaculatory
duct aedeagus
gonopore
paramere
paramere
primary phallic
lobe mesomere phallotreme
1956, for terminology) and the problems of homologizing is protected from injury in various ways. In grasshoppers
the different structures are outlined by Scudder (1971). and fulgorids, the sternum of the last abdominal segment
According to Snodgrass (1957) the basic elements are extends to form a subgenital plate (see Fig. 11.7a). In many
derived from a pair of primary phallic lobes which are Endopterygota, protection is afforded by withdrawal of the
present in the posterior ventral surface of segment 9 of the genital segments within the preceding abdominal seg-
embryo (Fig. 12.7a). They are commonly regarded as ments.
representing limb buds and the structures arising from Other components of the male external genitalia are
them as derived from typical appendages. Snodgrass concerned with grasping the female. They are often called
(1957), however, believes that they may represent ancestral claspers. They may be derived from the parameres, from
penes rather than appendages of segmental origin. These cerci, as in Dermaptera and many Orthoptera, or from the
phallic lobes divide to form an inner pair of mesomeres paraprocts, as in Zygoptera and some Tridactyloidea. In
and outer parameres, collectively known as the phallom- many Plecoptera, and occasionally in other orders, there
eres (Fig. 12.7b). The mesomeres unite to form the aedea- are no claspers, the sexes being held together by the fit of
gus, the intromittent organ. The inner wall of the the intromittent organ into the female bursa.
aedeagus, which is continuous with the ejaculatory duct, is Many male Diptera have the terminal abdominal seg-
called the endophallus, and the opening of the duct at the ments rotated so that the relative positions of the genitalia
tip of the aedeagus is the phallotreme (Fig. 12.7c). The are altered. In Culicidae, some Tipulidae, Psychodidae,
gonopore is at the outer end of the ejaculatory duct where Mycetophilidae and some Brachycera, segment 8 and the
it joins the endophallus and hence is internal, but in many segments behind it rotate through 180 ° soon after eclo-
insects the endophallic duct is eversible and so the gono- sion. As a result, the aedeagus comes to lie above the anus
pore assumes a terminal position during copulation. The instead of below it and the hindgut is twisted over the
parameres develop into claspers, which are very variable in reproductive duct (Fig. 12.8a). The rotation may occur in
form. They may be attached with the aedeagus on a either a clockwise or an anticlockwise direction. In
common base, the phallobase, and in many insects these Calliphora, and probably in all Schizophora, the terminal
basic structures are accompanied by secondary structures segments are rotated through 360 ° in the pupa so that the
on segments 8, 9 or 10. The term phallus is used by genitalia are in their normal positions at eclosion, but the
Snodgrass (1957) to mean the parameres together with the movement is indicated by some asymmetry of the pre-
aedeagus, but is often used to mean the aedeagus alone; ceding sclerites and by the ejaculatory duct looping right
penis is sometimes used instead of phallus. round the gut (Fig. 12.8b). The extent to which different
No intromittent organ is present in Collembola or segments rotate varies in different groups. Amongst the
Diplura. Male Archaeognatha and Thysanura have termi- Syrphidae, a total twist of 360 ° is achieved by two seg-
nal segments similar to those in females, but with a median ments rotating through 90 ° and one through 180 ° so that
phallus which is bilobed in Thysanura. In these groups, there is an obvious external asymmetry. Temporary rota-
sperm are not transferred directly to the female (see tion of the genital segments during copulation occurs in
section 12.3.3.1). Paired penes are present in some other insects, such as Heteroptera (Fig. 12.10).
Ephemeroptera and some Dermaptera, but in the majority Male Odonata differ from all other insects in having the
of pterygote insects there is a single median aedeagus. This intromittent organs on abdominal segments 2 and 3.
278 REPRODUCTIVE SYSTEM: MALE
female gonopore in
contact with male
accessory genitalia
head of thorax of
female female
c)
tergum 1 (seen
from inside) sternum 3
thorax of the female. This completed, he lets go with his into the male’s anal depression. The male uses his cerci to
legs and the two insects fly off ‘in tandem’. The claspers hold the female’s abdomen and the aedeagus is inserted
consist of superior and inferior pairs and, in Anisoptera, between the ventral valves of the ovipositor.
the superior claspers fit round the neck of the female while The male of Oncopeltus mounts the female, the genital
the inferior claspers press down on top of her head (Fig. capsule is rotated through 180 °, mainly by muscular action,
12.9b). In most Zygoptera, the claspers grip a dorsal lobe and the male’s parameres (claspers) grasp the female’s
of the pronotum and, in some Coenagriidae, they appear to ovipositor valves. Following insertion of the aedeagus, the
be cemented on by a sticky secretion (Corbet, 1983). insects assume an end to end orientation in which they are
Copulation may occur immediately after the insects held together mainly by the aedeagus (Fig. 12.10). An end to
have paired or there may be a considerable interval before end position is also taken up by Blattella (Blattodea), but at
they copulate. In the cockroach, Eurycotis, where the first the female climbs on the back of the male, who engages
female climbs on the male’s back, the signal that the insects the hook on his left phallomere on a sclerite in front of the
are in an appropriate position for copulation comes from ovipositor. Then, in the end to end position, the lateral
mechanosensitive hairs on the male’s first abdominal hooks on either side of the anus and a small crescentic scle-
tergite. The hairs are stimulated when the female attempts rite take a firm grip on the ovipositor (Fig. 12.11).
to feed on a secretion produced by glands close to the hairs Copulation in Odonata involves the male flexing his
and this only occurs when she is appropriately placed for abdomen so that the head of the female touches his acces-
the male to copulate (Farine et al., 1996). Once the male sory genitalia; she then brings her abdomen forwards
and female genitalia are linked, the insects may alter their beneath her so as to make contact with the accessory geni-
positions and it is common among Orthoptera and Diptera talia (Fig. 12.9a,c). Some species, such as Crocothemis, cop-
for an end to end position to be adopted at this time. ulate and complete sperm transfer in flight and, in these
The details of copulation vary from group to group insects, copulation is brief, lasting less than 20 s. Many
depending on the structure of the genitalia, and only a few species, however, settle before copulating and the process
examples are given. In Acrididae, the tip of the male’s may last for a few minutes or an hour or more. During most
abdomen is twisted below the female and the edges of the of this time, the male is removing sperm already present in
epiphallus (a plate on top of the genital complex) grip the the female’s spermatheca; sperm transfer takes only a few
sides of the female’s sub-genital plate and draw it down seconds (Corbet, 1980).
280 REPRODUCTIVE SYSTEM: MALE
a) anus
aedeagus
phallobase rectum
arm of subgenital
phallic pivot gland
erection fluid
pump
ejaculatory duct
(cut)
b) female male
rectum
spermatheca
vas deferens
lateral
oviduct
aedeagus anus subgenital accessory erection fluid
median oviduct genital gland glands reservoir
(cut open) chamber
Fig. 12.10. Male genitalia and direct insemination (Oncopeltus, Hemiptera) (after Bonhag & Wick, 1953). (a) Sagittal section
of the male genital capsule with the aedeagus retracted. (b) Sagittal section through the terminal segments of a copulating
pair. Notice the inversion of the male genital capsule (with the anus now ventral to the phallic pivot) and the insertion of the
aedeagus into the spermatheca.
The duration of copulation in other insects is equally in the female’s spermatheca. Sperm may be transferred in
variable. In mosquitoes the process is complete within a a spermatophore produced by the male, or they may be
few seconds, while in Oncopeltus the insects may remain passed directly into the spermatheca without a sper-
coupled for five hours, in Locusta for eight to ten hours, matophore being produced.
and in Anacridium (Orthoptera) for up to 60 hours.
Insemination is completed much more rapidly than this; in 12.3.3.1 Spermatophores
Locusta sperm reach the spermatheca within two hours of The primitive method of insemination in insects involves
the start of copulation. the production by the male of a spermatophore, a capsule in
which the sperm are conveyed to the female.
12.3.3 Insemination Spermatophores, of varying complexity, are produced by
In the insects, the transfer of sperm to the female (insemi- the Apterygota, Orthoptera, Blattodea, some Heteroptera,
nation) is a quite separate process from fertilization of the all the Neuroptera except Coniopterygidae, some
eggs, which in some cases does not occur until months or Trichoptera, Lepidoptera, some Hymenoptera and
even years later. During this interval the sperm are stored Coleoptera and a few Diptera Nematocera and Glossina.
TRANSFER OF SPERM TO THE FEMALE 281
female male will be eaten by himself and other insects. Male Lepisma
(Thysanura) also deposit spermatophores on the ground,
ovipositor but only in the presence of females. The male spins silk
crescentic
sclerite right phallomere threads over the female, making side to side movements
with his abdomen, so that her movements are restricted,
and she is then guided over the spermatophore, which she
inserts into her genital duct. In Machilis (Archaeognatha),
sternum
sternum sperm-containing droplets are deposited on a thread and
the male then twists his body round the female, guiding
her genitalia with his antennae and cerci into positions in
left phallomere
which they can pick up the droplets (Schaller, 1971).
transverse In the Pterygota, spermatophores are passed directly
sclerite from the male to the female. Where the spermatophore is
Fig. 12.11. Male genitalia. Ventral view of the terminal segments produced outside the female, one or two sperm sacs may be
of a male and female cockroach (Blattella) showing the manner embedded, or closely associated with, a gelatinous pro-
in which the male genitalia clasp the female. The insects are teinaceous mass called the spermatophylax (Fig. 12.12b).
represented in the end-to-end position with the subgenital plates In phasmids, gryllids and tettigoniids only the neck of the
and endophallus of the male removed. Female reproductive spermatophore penetrates the female ducts, the body of
sclerites, light stippling; male reproductive sclerites, dark the structure remains outside and is liable to be eaten by
stippling (after Khalifa, 1950).
the female or other insects (see below). In Blattodea the
body of the spermatophore, although still outside the
The spermatophore may be little more than a drop of female ducts, is protected by the female’s enlarged sub-
sperm-containing fluid deposited in the environment, but genital plate. The signal to transfer a spermatophore is
more usually it is a discrete structure that may be preformed provided to a male cricket by mechanical stimulation of
by the male and deposited on the female, or produced by the small trichoid sensilla in a cavity enclosed by his epi-
male when he encounters a female, or produced by male phallus. These hairs are stimulated by the female’s copula-
secretions in the female ducts during copulation. tory papillae when the insects copulate (Sakai et al., 1991).
The spermatophore is specialized in some Acrididae to
Structure and transmission In Collembola, the male form a tube which is effectively a temporary elongation of
deposits spermatophores on the ground quite inde- the intromittent organ (Fig. 12.12c). It consists of two
pendently of the presence of a female. The spermatophore basal bladders in the ejaculatory and sperm sacs of the
consists of a sperm-containing droplet, without any sur- male (Fig. 12.13) leading to a tube which extends into the
rounding membrane, mounted on top of a stalk which is female’s spermathecal bulb.
often about 500 m high. Sometimes spermatophores are In most other insect groups, many species practice
produced in aggregations of Collembola, so there is a good direct insemination without producing a spermatophore.
chance of a female finding one and inserting it into her Where a spermatophore is retained, it is often formed in
reproductive opening, while, in other cases, the male the female’s bursa copulatrix.
grasps the female by her antennae and leads her over the
spermatophore. The spermatophores of Campodea Spermatophore production The spermatophore is pro-
(Diplura) are also produced in the absence of the female duced from secretions of glands of the male’s reproductive
and, like those of Collembola, each one consists of a system, usually the accessory glands, but where these are
globule 50–70 m in diameter mounted on a peduncle absent or reduced, from glands in the ejaculatory duct (or
50–100 m high (Fig. 12.12a). The globule has a thin wall the simplex in Lepidoptera). The secretions are molded in
which encloses a granular fluid, floating in which are from the ducts of the male and sometimes also the female.
one to four bundles of sperm. The sperm can survive in a Secretions from different glands, or different cells within a
spermatophore for two days. A male may produce some gland, are produced in sequence to form separate parts of
200 spermatophores in a week, but at least some of these the spermatophore.
282 REPRODUCTIVE SYSTEM: MALE
a) Campodea c) Locusta
coils of distal
tube
spermatheca
ball of in female
sperm
seminal fluid distal tube
50 µm
peduncle
proximal
tube
in male
b) Blattella
second bladder
Fig. 12.12. Spermatophores. (a) Produced independently of the female and left on the ground (Campodea, Diplura) (after
Bareth, 1964). (b) Deposited at the opening of the female duct (Blattella, Blattodea) (after Khalifa, 1950). (c) Produced
within the male and female ducts during copulation and connecting directly with the spermatheca. See Fig. 12.13(a) for
details of male genitalia (Locusta, Orthoptera) (after Gregory, 1965).
Production of the spermatophore by Locusta begins part of the proximal tube enters the bladder it draws the
within two minutes of the start of copulation. Most of it is wall of the reservoir tube with it, so that this becomes
formed in the male, although the ducts of the female serve invaginated, and finally the whole of the tube except for
to mold the tubular part. The first secretion builds up in the tip is pushed inside the bladder by a mucilaginous
the upper ejaculatory duct and is forced down through the secretion (Fig. 12.13e).
funnel, the shape of which produces a series of folds, At this time the ejaculatory sac starts to contract and
molding the secretion into a cylinder (Fig. 12.13). A white squeezes the tube of the spermatophore out of the bladder,
semi-fluid secretion is then forced into the core of the while the pressure of mucilage in the ejaculatory duct
cylinder so that it becomes a tube (Fig. 12.13b). This is forces the tip backwards through the gonopore, which is
enlarged in the ejaculatory sac to form the first bladder, now open, and out through the aedeagus into the duct of
while the part remaining in the ejaculatory duct (known at the female’s spermatheca (Fig. 12.13f,g). This process
this time as the reservoir tube) ultimately forms the second involves the tube being turned inside out and finally the
bladder in the spermatophore sac. At this stage seminal second bladder is everted and molded in the sperm sac (see
fluid is passed into the rudimentary spermatophore and Gregory, 1965 for a full account of this process). In
then a separate cylinder of material is formed and pushed Gomphocerus, the tube is not turned inside out, but elon-
into the bladder, where it becomes coiled up (Fig. 12.13c). gates by expansion (Hartmann, 1970).
This will form the distal tube and a further series of secre- The spermatophore of Lepidoptera is formed wholly
tions forms the proximal tube (Fig. 12.13d). As the last within the female ducts after the start of copulation. Here,
TRANSFER OF SPERM TO THE FEMALE 283
first bladder
distal tube
the different glands function in sequence, starting with the duct to the female’s bursa copulatrix (Osanai, Kasuga &
section of the simplex nearest the aedeagus (Fig. 12.14). Aigaki, 1987, 1988; and see Fanger & Naumann, 1993).
The aedeagus projects into the female’s bursa copulatrix For an account of the production of a spermatophore
and the secretion of the lower region of the simplex forms a from multiple secretions of the accessory glands of
pearly body (not shown in Figure) and the wall of the sper- Tenebrio see Dailey, Gadzama & Happ (1980) and refer-
matophore. This is followed by the contents of the seminal ences cited in Happ (1984).
vesicle, the sperm and seminal fluid, partly mixing with Reviews: Mann, 1984; Tuzet, 1977b
them to form the inner matrix of the spermatophore. The
secretion from the lower parts of the accessory glands forms Transfer of sperm to the spermatheca Immediately fol-
the outer matrix, and, finally, the secretions from the ends lowing the transfer of the spermatophore, the sperm
of the glands form the spermatophragma which blocks the migrate to the spermatheca, where they are stored.
284 REPRODUCTIVE SYSTEM: MALE
Fig. 12.14. ABOVE: male and part of the female reproductive systems of the silkmoth, Bombyx, showing how secretions from
different parts of the male system contribute to different parts of the spermatophore (shown by corresponding shading). Note
that the female system is shown at a much larger scale. Numbers show the sequence in which secretions are produced from
different regions (based on Osanai, Kasuga & Aigaki, 1987, 1988). BELOW: chemical reactions occurring in the spermatheca
which produce the respiratory substrate for sperm activity.
Sometimes they are able to escape from the sperm sac The transfer of sperm to the spermatheca may be
through a pore, but in other cases, where the sperm sac is either active or passive. In Acheta, sperm are held in the
completely enclosed within the spermatophore, they body of the spermatophore (the ampulla), which remains
escape as a result of the spermatophore rupturing. In external to the female, and the spermatophore is special-
Lepidoptera and Sialis, the inside of the bursa copulatrix ized to force the sperm out into the female ducts. An outer
is lined with spines or bears a toothed plate, the signum reservoir of fluid, the evacuating fluid, with a low osmotic
dentatum, to which muscles are attached. The sper- pressure is separated by an inner layer with semipermeable
matophore is gradually abraded by movements of the properties from an inner proteinaceous mass called the
spines until it is torn open. In Rhodnius, the first sperm pressure body, which has a high osmotic pressure (Fig.
reach the spermatheca within about 10 minutes of the end 12.15a). When the spermatophore is deposited, water
of mating, while in Acheta transfer takes about an hour, and passes from the evacuating fluid into the pressure body
in Zygaena (Lepidoptera) 12–18 hours. because of the difference in osmotic pressure. The
TRANSFER OF SPERM TO THE FEMALE 285
a) b)
pressure body
producing
outer layer transparent
material
evacuating fluid
pressure body
granular
substance
tails of
sperm c) d)
heads of
sperm
transparent
material
proximal end of granular
tube substance
sperm forced
out
Fig. 12.15. Spermatophore of the house cricket (Acheta, Orthoptera) (after Khalifa, 1949). (a) Horizontal section through the
ampulla which remains outside the female. (b) The pressure body starts to swell and releases a transparent material due to the
absorption of evacuating fluid from outside the inner layer. In (b)–(d), the outer layer and evacuating fluid are not shown. (c)
Production of the transparent material continues starting to push sperm out of the ampulla. (d) Sperm have been completely
forced out of the ampulla.
pressure body produces a transparent material and swells, sperm are taken into the oviduct. As this process contin-
forcing the sperm out of the ampulla and down the tube of ues, the more anterior sperm are forced forwards along the
the spermatophore into the spermatheca (Fig. 12.15b–d). oviduct and are passed into the spermatheca. In Diptera
In Locusta, also, the sperm in the spermatophore are ini- Nematocera, it is probable that fluid is absorbed from the
tially outside the female (in this case, in the first bladder of spermatheca creating a current which transports the
the spermatophore). From here they are pumped along sperm into the spermatheca (Linley & Simmonds, 1981).
the spermatophore by contractions of the ejaculatory sac, In contrast to these examples, however, the sperm of
first appearing in the spermatheca about 90 minutes after Bombyx are activated before they leave the spermatophore
the start of copulation. (see below), and they may contribute actively to their
In many insects the spermatophore is placed in the transfer to the spermatheca.
bursa copulatrix of the female and the transfer of sperm to
the spermatheca is probably brought about by the contrac- Fate of the spermatophore Females of some species eject
tions of the female ducts. An opaque secretion from the the spermatophore some time after insemination. Blattella
male accessory glands of Rhodnius injected into the bursa and Rhodnius, for instance, drop the old spermatophores
with the spermatophore induces rhythmic contractions of some 12 and 18 hours, respectively, after copulation. The
the oviducts, probably by way of a direct nervous connec- female Sialis pulls the spermatophore out and eats it and
tion from the bursa to the oviducal muscles. The contrac- this commonly happens in Blattodea, where specific post-
tions cause shortening of the oviduct, and, it is suggested, copulatory behavior often keeps the female occupied for a
cause the origin of the oviduct in the bursa to make bite- time to ensure that the sperm have left the spermatophore
like movements in the mass of semen in the bursa so that before she eats it. In some grasshoppers, such as
286 REPRODUCTIVE SYSTEM: MALE
a) Xylocoris
sperm moving through
tergum 2 tergum 3 conducting lobe
conducting lobe of
mesospermalege
ectospermalege sperm in
hemocoel
sperm in receiving
lobe
b) Orius c) Orius
ovary lateral oviduct
(left)
sperm in
conducting tissue of conducting tissue
mesospermalege
base of right
oviduct (cut)
gonopore
sperm
pouch
sternum 8 sperm
pouch end of copulatory
copulatory copulatory sternum 7 tube
tube opening
Fig. 12.16. Hemocoelic insemination in Hemiptera. Arrows show direction of sperm movement. (a) Longitudinal section
through the ectospermalege and mesospermalege of Xylocoris galactinus about one hour after copulation (after Carayon,
1953a). (b) Diagram of the internal reproductive organs of female Orius. (c) Longitudinal section of part of the
mesospermalege of Orius showing the sperm pouch and conducting tissue (after Carayon, 1953b).
Gomphocerus, the spermatophore is ejected by muscular Locusta breaks when the two sexes separate, either where
contraction of the spermathecal duct. the tube fits tightly in the spermathecal duct or at its origin
The spermatophore is dissolved by proteolytic with the bladders in the male. The part remaining in the
enzymes in other insects, such as Lepidoptera and male is ejected within about two hours by the contractions
Trichoptera, and in many Trichoptera only the sperm sac of the copulatory organ, while in the female the distal tube
remains one or two days after copulation. In the wax moth, disappears within a day, presumably being dissolved, but
Galleria, digestion is complete in ten days, but the neck of the proximal tube dissolves much more slowly, and persists
the spermatophore persists. The spermatophore of for several days until it is ejected, probably by contractions
TRANSFER OF SPERM TO THE FEMALE 287
of the spermathecal duct. In Chorthippus the activity of the the vagina, but a spine at its tip perforates the wall of the
enzyme-secreting cells of the spermatheca is controlled by vagina so that the sperm are injected into the hemocoel.
the corpora allata. They are not phagocytosed immediately, but disperse
beneath the integument and later collect under the peri-
12.3.3.2 Direct insemination toneal membrane surrounding the ovarioles, possibly
Various groups of insects have dispensed with a sper- being directed chemotactically. The sperm adjacent to the
matophore and sperm are transferred directly to the lowest follicle penetrate the follicular epithelium and fer-
female ducts, and often into the spermatheca, by the penis, tilize the eggs via the micropyles.
which may be long and flagelliform for this purpose. Such Primicimex shows a further separation from the normal
direct insemination occurs in some members of the orders method of insemination. Here the left clasper of the male
Heteroptera, Mecoptera, Trichoptera, Hymenoptera, penetrates the dorsal surface of the abdomen of the female,
Coleoptera and Diptera. usually between tergites 4 and 5 or 5 and 6. The clasper
Direct insemination occurs in Aedes aegypti, and, in ensheathes the penis, and sperm are injected into the
this insect, the paraprocts expand the genital orifice of the hemocoel. They accumulate in the heart and are distrib-
female while the aedeagus is erected by the action of uted round the body with the blood. Many are phagocy-
muscles attached to associated apodemes. The aedeagus tosed by the blood cells, but those that survive are stored in
only penetrates just inside the female opening, where it is two large pouches at the base of the oviducts. The holes
held by spines engaging with a valve of the spermatheca. A made in the integument by the claspers become plugged
stream of fluid from the accessory glands is driven along with tanned cuticle.
the ejaculatory duct and into the female by contractions of In other species, the sperm are not injected directly
the glands, and sperm are injected into the stream by the into the hemocoel, but are received into a special pouch
contractions of the seminal vesicles. Thus a mass of semen called the mesospermalege or organ of Ribaga or Berlese,
is deposited inside the atrium of the female and from here which is believed to be derived from blood cells. Other
the sperm are transferred to the spermatheca. The sperm genera have a cuticular pouch, called the ectospermalege,
of Drosophila are similarly deposited in the vagina and then for the reception of the clasper and the penis. There may
pass to the spermatheca. be one or two ectospermalegia and their positions vary, but
Oncopeltus has a long penis which reaches into the sper- in Afrocimex they are situated in the membrane between
matheca and deposits sperm directly into it (Fig. 12.10). segments 3 and 4 and segments 4 and 5 on the left-hand
Erection of the phallus in this insect is a specialized mech- side. Xylocoris galactinus has a mesospermalege for the
anism involving the displacement of an erection fluid into reception of sperm immediately beneath the
the phallus from a reservoir of the ejaculatory duct. The ectospermalege (Fig. 12.16a). The mesospermalege is
fluid is forced back from the reservoir by pressure exerted formed from vacuolated cells surrounding a central lacuna
by the body muscles, and this pressure is maintained into which the sperm are injected and from here they move
throughout copulation. At the end of the ejaculatory duct, down a solid core of cells, forming the conducting lobe,
the fluid is forced into a vesicle and then pumped into the into the hemocoel. They finally arrive at the conceptacula
phallus. In those Coleoptera and Hymenoptera with a long seminis at the bases of the lateral oviducts, where they
penis, erection is probably produced by an increase in accumulate. In Cimex this migration takes about 12 hours
blood pressure resulting from the sudden contraction of and after the female takes her next blood meal the sperm
the abdominal walls. are carried intracellularly in packets to the ovaries through
special conduit cells. At the base of each ovariole they
12.3.3.3 Hemocoelic insemination accumulate in a corpus seminalis derived from the follicu-
In some Cimicoidea (Hemiptera), the sperm, instead of lar cells (Davis, 1964).
being deposited in the female reproductive tract, are In Anthocoris and Orius, perforation of the integument
injected into the hemocoel. A good deal of variation occurs is not necessary because a copulatory tube opens on the left
between the species practicing this method and they can be between the sternites of segments 7 and 8 and passes to a
arranged in a series showing progressive specialization median sperm pouch, where the sperm accumulate (Fig.
(Hinton, 1964). In Alloeorhynchus flavipes the penis enters 12.16b,c). From here the mesospermalege forms a column
288 REPRODUCTIVE SYSTEM: MALE
of conducting tissue along which the sperm pass to the a) number of oocytes
oviducts, so that they are never free in the hemocoel. 15
In all these examples some sperm are digested by blood
cells or by phagocytes in the mesospermalege. They prob-
ably have nutritional value, and perhaps hemocoelic 10
number
insemination and its associated digestion of sperm facili-
tates more prolonged survival of the recipients in the
5
absence of food (Hinton, 1964), although this has been
questioned by other authorities (see Leopold, 1976).
In Strepsiptera, sperm also pass into the hemocoel to 0
fertilize the eggs, but they do so via the genital canals of the 0 20 40 60 80
female (see Fig. 14.31).
Review: Carayon, 1977 b) egg weight
1.3
weight (mg)
1.2
In the course of sperm transfer, secretions of the male
accessory glands are transferred to the female and these
may have various effects on her subsequent behavior and 1.1
physiology.
a) Teleogryllus b) Delia
mated
unmated mated injected
15
20
10
eggs/day
number
10
5
0 0
5 10
days
mated days 1-4
unmated days 5-15
Fig. 12.18. Enhancement of oviposition as a result of mating and transfer of male accessory gland material to the female. (a)
Number of eggs per day laid by females of the Australian field cricket, Teleogryllus after mating. Unmated females lay only a
few eggs each day (after Stanley-Samuelson, 1994). (b) Average number of eggs per day laid by females of the onion fly, Delia
when unmated, mated or after injection of an extract of male accessory glands into unmated females. Bars show averages for
the first four days and the next 11 days (data from Spencer et al., 1992).
Padgham, 1973). A single spermatophore contains trigger for oviposition and sometimes oogenesis. Virgin
sufficient sperm to fertilize several batches of eggs and it is females usually do not lay eggs, or lay relatively few.
possible that mating after the first oviposition is more Mating, or the experimental injection of a component of
important in maintaining fecundity than in maintaining the male accessory glands, causes them to oviposit (Fig.
fertility (Leahy, 1973). Although only one spermatophore 12.18).
is produced each time Chorthippus mates, repeated mating In Drosophila and the beetle, Acanthoscelides, the fertil-
by the female enhances both the rate of egg production and ity-enhancing compound is a peptide. That in Drosophila
the number of eggs per pod irrespective of whether the contains 36 amino acids (Kubli, 1992). In some other
insects have ample food or only a limited supply (Butlin, insects, grasshoppers, crickets and a mosquito, the active
Woodhatch & Hewitt, 1987). There is also evidence that compound is known to be a protein. In addition, males of
multiple mating by Drosophila mojavensis contributes some crickets and lepidopterans transfer prostaglandins or
material for oogenesis (Markow & Ankney, 1984). prostaglandin-synthesizing chemicals to the female during
Some butterflies exhibit puddling behavior, aggregat- copulation. These have also been shown to stimulate
ing at muddy pools and drinking. A principal function of oviposition (Stanley-Samuelson, 1994).
this behavior is to accumulate sodium. In many species, only Within the female, the peptides and proteins may act in
males exhibit this behavior and they may be anatomically, one of two ways. Either they may stimulate the tissue of
and presumably physiologically, adapted to accumulate the reproductive tract to produce a hormone, or they may
sodium which they then transfer to the females during enter the hemocoel and affect a distant target site. In
copulation. Males of the skipper butterfly, Thymelicus Rhodnius, the fertility-enhancing factor induces the tissues
lineola, transfer more than 10% of their body weight as of the spermatheca and associated ducts to produce a
sodium to females in this way. The sodium increases female hormone, known as the spermathecal factor. This causes
fertility (Pivnick & McNeil, 1987; Smedley & Eisner, 1995). some neurosecretory cells in the brain to release a peptide
that produces contractions of the ovarian sheath leading to
12.4.2 Enhancement of female fertility ovulation (Kriger & Davey, 1984).
In addition to the possible nutrient effects that accompany The sex peptide of Drosophila is derived from a larger
sperm transfer in many insects, copulation may also be a peptide transferred to the female and then cleaved in the
290 REPRODUCTIVE SYSTEM: MALE
bursa copulatrix. After absorption into her hemolymph, it further mating by the female. It may also ensure that
acts directly on the brain, at least with respect to its func- sperm in the bursa copulatrix are transferred to the sper-
tion in inhibiting female receptivity (see below). The matheca rather than moving back towards the vulva.
fecundity enhancing compound produced by Bombyx acts Loss of receptivity by the female is sometimes regu-
directly on the terminal abdominal ganglion. lated directly through neural pathways. For instance,
In the mosquito, Aedes aegypti, a secretion from the females of Nauphoeta and Gomphocerus are unreceptive
male accessory glands also induces the female to respond while there is a spermatophore in the spermatheca;
to the stimuli of potential oviposition sites to which she cutting the ventral nerve cord results in the return of
was previously unresponsive (Yeh & Klowden, 1990). receptivity. In Aedes, receptivity is also first switched off by
mechanical stimulation resulting from filling the bursa
12.4.3 Reduction of female’s readiness to remate copulatrix with seminal fluid. Subsequently, however, the
Males of many species employ some mechanism to reduce female remains unreceptive for the rest of her life as a
the likelihood that a female with whom he has just mated result of a substance, known as matrone, in the secretions
will mate again. This may take the form of mate guarding, of the male accessory glands. Matrone passes from the
but often involves a male-induced effect on the female’s bursa copulatrix into the hemolymph and then acts
ability or willingness to mate again. In some species, the directly on the central nervous system of the female.
reduction in receptivity is permanent and the female never Receptor sites probably exist in the terminal abdominal
mates again; in others, receptivity subsequently returns. ganglion (Leopold, 1976). The male accessory gland
Species in which the female mates only once are common secretions also affect host-seeking by female mosquitoes
amongst Hymenoptera and Diptera. The solitary bee (Fernandez & Klowden, 1995). A sex peptide also
(Centris pallida), the onion fly (Delia antiqua) and tsetse switches off female receptivity in Drosophila, but the sus-
flies (Glossina), are examples. Similar behavior is recorded tained depression of sexual activity over a period of days is
in a few species from other orders. Cyclical changes in probably dependent on the presence of sperm in the sper-
receptivity, resulting from the resumption of mating after matheca (Kubli, 1992).
an interval, occur in many species in most insect orders, In the housefly, Musca, and the stable fly, Stomoxys,
often in relation to the female’s cycle of oogenesis. Female where accessory glands are absent, a secretion from the
Drosophila melanogaster will remate about a week after a ejaculatory duct inhibits female receptivity (see below)
previous mating (Spencer et al., 1992). (Morrison, Venkatesh and Thompson, 1982). Compounds
These changes in female behavior induced by the male that inhibit receptivity are also known to occur in
may be associated with the physical blocking of the female Lepidoptera.
ducts by the spermatheca or some other component of the Not only is female receptivity reduced, in Helicoverpa
male accessory gland secretion forming a mating plug. In some chemical component of the spermatophore leads to
other instances, components of the male accessory gland an immediate reduction in the synthesis of sex attractant
secretion affect female behavior without physically pre- pheromone by the female (Fig. 12.19) (Kingan, Thomas-
venting further sperm transfer. Laemont & Raina, 1993).
Mating plugs, distinct from spermatophores, are pro-
duced in a number of insects. Thus, in mosquitoes belong- 12.4.4 Transfer of other ecologically relevant
ing to the genera Anopheles, Aedes and Psorophora, a plug, compounds
formed from the accessory gland secretions of the male, is Some examples are known of males transferring chemicals
deposited in the genital chamber of the female, even which have ecological relevance to the species beyond the
though these insects do not produce a spermatophore. A immediate context of reproduction. For example, males of
similar plug is produced by some species of Drosophila the ‘Spanish fly’ (Lytta, Coleoptera) synthesize can-
(Alonso-Pimentel, Tolbert & Heed, 1994) and by the hon- tharidin, presumably as a defensive substance. It is proba-
eybee, Apis. A comparable structure is present in some bly synthesized and stored in the accessory reproductive
Lepidoptera where it is produced immediately after the glands. Females do not synthesize the compound, but large
spermatophore (Fig. 12.14). It is called the sper- quantities are transferred to the female during copulation
matophragma or sphragis and it effectively prevents (Sierra, Woggon & Schmid, 1976).
SPERM CAPACITATION 291
a) after normal mating at the plant surface. In both species, males transfer large
amounts of these compounds to the females during
unmated copulation. They are subsequently found in the eggs
100 where they have been shown to have a protective function
unmated
-1
100
of maximum)
75
50 to the female (LaMunyon & Eisner, 1994).
50
(% of(%
25
12.5 SPERM CAPACITATION
25
0
0 60 120
In a number of species, sperm undergo changes after they
0 time since mating (min) are transferred to the female spermatheca and in some
0 60 120 cases, at least, these changes are essential before the sperm
time since mating (min) can fertilize an egg. This process of maturation of sperm
within the female is known as capacitation. In Musca, the
b) after injection of sperm lose the plasma membrane from the head and most
accessory gland of the granular material from the acrosome.
extract More obvious changes occur where the sperm are still
control injected grouped together when they leave the spermatophore. In
100 grasshoppers, the glycoprotein binding the sperm
together is dissolved in the spermatheca so that they separ-
75 ate. The glycocalyx is also removed. This occurs within 6
hours in one part of the spermatheca, in another part it
50 takes more than 15 hours from the time of insemination.
Sperm from this region are those that will ultimately fer-
25 tilize the eggs (Longo et al., 1993).
The breakup of bundles of eupyrene sperm in the sper-
0 matophore of Lepidoptera is associated with, and probably
caused by the activation of apyrene sperm. A specific pro-
Fig. 12.19. Reduction in pheromone production as a result of
tease from the lower simplex digests the glycoprotein cov-
mating and transfer of male accessory gland material to the
female of the moth, Helicoverpa. (a) Reduction in the amount of ering the flagellar membrane of the apyrene sperm. The
the sex attractant pheromone component, Z-11-hexadecanal, in same protease liberates arginine from proteins in the
the female following mating (after Raina, 1989). (b) Effect of seminal fluid, and the arginine is metabolized to 2-oxoglu-
injecting an extract of the male accessory glands on the amount of tarate, a preferred substrate for the sperm (Fig. 12.14)
Z-11-hexadecanal in the female (data from Kingan et al., 1993). (Aigaki, Kasuga & Osanai, 1987; Osanai & Kasuga, 1990).
Cyclic AMP is also necessary to activate the sperm. Once
the apyrene sperm of Bombyx are activated, they appear to
A similar transfer of compounds that confer protection break up the eupyrene sperm bundles by their physical
against predators is known to occur in some Lepidoptera. activity. A protease liberating arginine and cAMP are also
Larvae of the moth, Utetheisa, feed on plants containing necessary for sperm activation in grasshoppers (Osanai &
pyrrolizidine alkaloids, and adult males of the milkweed Baccetti, 1993; Osanai & Kasuga, 1990).
butterfly, Danaus, obtaining the same chemicals by licking
292 REPRODUCTIVE SYSTEM: MALE
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Physiology, 35, 821–6. Cell and Tissue Research, 276, 15–21. Uvarov, B.P. (1966). Grasshoppers and
Riemann, J.G. & Giebultowicz, J.M. Smedley, S.R. & Eisner, T. (1995). Locusts, vol. 1. Cambridge: Cambridge
(1991). Secretion in the upper vas Sodium uptake by puddling in a moth. University Press.
deferens of the gypsy moth correlated Science, 270, 1816–8. Wigglesworth, V.B. (1965). The Principles
with the circadian rhythm of sperm Snodgrass, R.E. (1935). Principles of Insect of Insect Physiology. London: Methuen.
release from the testes. Journal of Insect Morphology. New York: McGraw-Hill. Yeh, C. & Klowden, M.J. (1990). Effects
Physiology, 37, 53–62. Snodgrass, R.E. (1957). A revised inter- of male accessory gland substances on
Sakai, M., Taoda, Y., Mori, K. Fujino, M. pretation of the external reproductive the pre-oviposition behavior of Aedes
& Ohta, C. (1991). Copulation organs of male insects. Smithsonian aegypti mosquitoes. Journal of Insect
sequence and mating termination in the Miscellaneous Collections, 135, no. 6, 60 Physiology, 36, 799–803.
male cricket Gryllus bimaculatus pp.
DeGeer. Journal of Insect Physiology, Spencer, J.L., Bush, G.L., Keller, J.E. &
37, 599–615. Miller, J.R. (1992). Modification of
Schaller, F. (1971). Indirect sperm trans- female onion fly, Delia antiqua
fer by soil arthropods. Annual Review of (Meigen), reproductive behavior by
Entomology, 16, 407–46. male paragonial gland extracts
(Diptera: Anthomyiidae). Journal of
Insect Behavior, 5, 689–97.
13 Reproductive system: female
13.1 ANATOMY OF THE INTERNAL ovary with a single ovariole. At the other extreme are the
REPRODUCTIVE ORGANS queens of some species of social insects: each ovary of the
queen termite, Eutermes, has over 2000 ovarioles, and that
The female reproductive system consists of a pair of
of a queen honeybee 150–180. Species which disperse as
ovaries, which connect with a pair of lateral oviducts.
first stage larvae may also have large numbers of ovarioles.
These join to form a median oviduct opening posteriorly
Scale insects have several hundred ovarioles and the blister
into a genital chamber. Sometimes the genital chamber
beetle, Meloe, 1000.
forms a tube, the vagina, and this is often developed to
Other than in Diptera, there is no sheath enclosing the
form a bursa copulatrix for reception of the penis.
ovary as a whole, but each ovariole has a sheath which is
Opening from the genital chamber or the vagina is a sper-
made up of two layers: an outer ovariole sheath, or tunica
matheca for storing sperm, and, frequently, a pair of acces-
externa, and an inner tunica propria (Fig. 13.4b,c). The
sory glands is also present (Fig. 13.1).
tunica externa is an open network of cells, sometimes
Review: Martoja, 1977
including muscle cells. The cells of this net are rich in
lipids and glycogen and are metabolically active, but there
Ovary The two ovaries lie in the abdomen above or lateral is no evidence that they are directly concerned with oocyte
to the gut. Each consists of a number of egg-tubes, or ovar- development. Tracheoles also form part of the external
ioles, comparable with the testis follicles in the male. The sheath, but they do not penetrate it and all the oxygen uti-
oocytes develop in the ovarioles. The ovaries of lized by the developing oocytes diffuses in from these ele-
Collembola are probably not homologous with those of ments. In Periplaneta, mycetocytes (section 4.3.2.2) are
insects, but are sac-like with a lateral germarium and no present in the sheath.
ovarioles. The tunica propria is a basal lamina with elastic proper-
The number of ovarioles in an ovary varies in relation ties possibly secreted by the cells of the terminal filament
to size and life style of the insect as well as its taxonomic and the follicle cells. It surrounds the whole of each ovari-
position. In general, larger species within a group have ole and the terminal filament. During the early stages of
more ovarioles than small ones; thus small grasshoppers development it increases in thickness, but during the
commonly have only four ovarioles in each ovary, while period of yolk uptake, when the oocytes enlarge rapidly, it
larger ones may have more than 100. Similarly, in the becomes stretched and very thin. The tunica propria has a
higher Diptera, Drosophila has 10–30 ovarioles in each supporting function, maintaining the shape of the ovari-
ovary, whereas Calliphora has about 100. By contrast, most ole, and, in addition, because of its elasticity, playing a part
Lepidoptera have four ovarioles on each side irrespective in ovulation (section 13.3). It also has the potential to func-
of their size. Variation in relation to size may also occur tion as a molecular sieve since, in Phormia, it does not
within a species. In the mosquito, Aedes punctor, the permit the passage of molecules larger than 500 kDa.
number of ovarioles in the two ovaries combined varies Each ovariole is produced, distally, into a long terminal
from about 30 to 175 as the insect’s size increases, but the filament consisting of a cellular core bounded by the tunica
cockroach, Periplaneta americana, has eight on each side propria (Figs. 13.1a, 13.4). Usually the individual
irrespective of its size. filaments from each ovary combine to form a suspensory
Viviparous species exhibit extreme reduction in the ligament and sometimes the ligaments of the two sides
numbers of ovarioles. The viviparous Diptera, merge into a median ligament. The ligaments are inserted
Melophagus, Hippobosca and Glossina, have only two in each into the body wall or the dorsal diaphragm and so suspend
ovary and some viviparous aphids have only one functional the developing ovaries in the hemocoel.
[295]
296 REPRODUCTIVE SYSTEM: FEMALE
a) Schistocerca b) Rhagoletis
oocyte in
terminal ovariole
filaments
accessory
gland calyx
spermatheca
accessory
gland
oocyte in
ovariole lateral
oviduct
median
oviduct
pedicel
lateral
oviduct
vagina
spermatheca
median
oviduct
Fig. 13.1. Female reproductive system (partly after Snodgrass, 1935). (a) An insect with many ovarioles opening sequentially
into the lateral oviducts. The oviduct and spermatheca open independently (Orthoptera: Schistocerca). (b) An insect in which
the ovarioles open together into the end of the lateral oviduct which forms the calyx. The genital chamber is a continuation of
the median oviduct, forming the vagina. The spermathecae arise at the junction of the vagina with the median oviduct
(Diptera: Rhagoletis).
Proximally, the ovariole narrows to a fine duct, the Oviducts The oviducts are tubes with walls consisting of a
pedicel, which connects with the oviduct. In an immature single layer of cuboid or columnar cells standing on a basal
insect the lumen of the ovariole is cut off from the oviduct lamina and surrounded by a muscle layer. Usually, the two
by an epithelial plug, but this is destroyed at the time of the lateral oviducts join a median oviduct which is ectodermal
first ovulation and subsequently is replaced by a plug of in origin and hence lined with cuticle. However, the
follicular tissue. Ephemeroptera are exceptional in having the lateral
The ovarioles may connect with the oviduct in a linear oviducts opening separately, each with its own gonopore.
sequence and, if there are only a few, as in some Apterygota The median oviduct is usually more muscular than the
and Ephemeroptera, they may appear to be segmental. lateral ducts, with circular and longitudinal muscles. It
This appearance is probably coincidental and there is no opens at the gonopore which, in Dermaptera, is ventral on
suggestion of a segmental arrangement in insects with a the posterior end of segment 7, but in most other groups
larger number of ovarioles (Fig. 13.1a). In other groups, opens into a genital chamber invaginated above the sternum
such as the Lepidoptera and Diptera, the ovarioles open of segment 8 (Fig. 13.2a). Sometimes the genital chamber
together into an expansion of the oviduct known as the becomes tubular and it is then effectively a continuation of
calyx (Fig. 13.1b). the oviduct through segment 9. Such a continuation is
ANATOMY OF THE INTERNAL REPRODUCTIVE ORGANS 297
rectum
oviduct
spermatheca
gonopore
anus
rectum
anus
genital oviporus
chamber
vagina
bursa sperm vulva
oviduct spermatheca gonopore copulatrix duct
sternum
8 segment segment
8 9 + 10
Fig. 13.2. Female reproductive system. Diagrammatic sagittal sections of the end of the abdomen. (a) An insect in which the
genital chamber is open, not tubular (Orthoptera: Locusta) (after Uvarov, 1966). (b) A ditrysian lepidopteran in which the
genital chamber forms the vagina (after Imms, 1957).
called the vagina and its opening to the exterior, the vulva three (Fig. 13.1b). In Orthoptera and other lower insects
(but notice the different terminology in ditrysian Lepi- orders, the spermatheca opens into the genital chamber
doptera, Fig. 13.2b). The vagina may not be distinguishable independently of the oviduct (Fig. 13.2a), but, where the
in structure from the median oviduct, but its anterior end, genital chamber forms a vagina, the spermathecal opening
and the position of the true gonopore, is marked by the is internal and is effectively within the oviduct (Fig.
insertion of the spermatheca (Snodgrass, 1935). 13.2b). The spermatheca is ectodermal in origin and is
Frequently the vagina is developed to form a pouch, the lined with cuticle. Typically it consists of a storage pouch
bursa copulatrix, which receives the penis, while in vivipar- with a muscular duct leading to it. A gland is often associ-
ous Diptera the anterior part of the chamber is enlarged to ated with it, or the spermathecal epithelium may itself be
form the uterus, in which larval development occurs. glandular. The contents of the spermatheca, derived from
The females of the ditrysian Lepidoptera are unusual the glands, are known to contain several proteins and
in having two reproductive openings (Fig. 13.2b). One, on include a carbohydrate–protein complex. The functions of
segment 9, serves for the discharge of eggs and is known as these secretions are not known for certain, but they proba-
the oviporus; the other, on segment 8, is the copulatory bly provide nutrients for the sperm during storage, or they
opening, known as the vulva. The latter leads to the bursa may be concerned with sperm activation (Gillott, 1988).
copulatrix which is connected with the oviduct by a sperm
duct. Two openings also occur in the water beetles Agabus, Accessory glands Female accessory glands often arise from
Ilybius and Hydroporus, but here both openings are termi- the genital chamber or the vagina. Where such glands are
nal with the bursa copulatrix opening immediately above apparently absent the walls of the oviducts may themselves
the vagina. be glandular. This is the case in grasshoppers where the
lateral oviducts also usually have a wholly glandular ante-
Spermatheca A spermatheca, used for the storage of rior extension (Fig. 13.1a).
sperm from the time the female is inseminated until the Accessory glands often produce a substance for attach-
eggs are fertilized, is present in most female insects. ing the eggs to the substratum during oviposition and
Sometimes there are two, as in Blaps (Coleoptera) and hence are often called colleterial (glue) glands. In a number
Phlebotomus (Diptera), and most of the higher flies have of insects, they produce an ootheca that protects the eggs
298 REPRODUCTIVE SYSTEM: FEMALE
after oviposition (section 13.5.4). Glands associated with The follicle cells also produce ecdysone, or a precursor of
the genitalia, which are often modified to form a sting, ecdysone, which, at least in some insects, accumulates in
perform a variety of functions in female Hymenoptera (see the oocyte (section 14.2.15 and see section 13.2.4.2). In the
Chapter 27). later stages of oogenesis, they produce the vitelline enve-
lope and the ligands responsible for determination of the
terminals of the embryo and its dorso-ventral axis (section
13.2 OOGENESIS
14.2.5). Finally, they produce the egg shell, or chorion
Each ovariole consists of a distal germarium in which (section 13.2.5).
oocytes are produced from oogonia, and a more proximal Each ovariole typically contains a linear series of
vitellarium in which yolk is deposited in the oocytes. oocytes in successive stages of development with the most
These two regions reflect two phases of oocyte growth: the advanced in the most proximal position furthest from the
first is regulated directly by the oocyte’s genome and con- germarium (Fig. 13.4). An oocyte with its surrounding fol-
tains species specific information (all the substances whose licular epithelium is termed a follicle and successive folli-
synthesis is regulated by the DNA of the germ line are cles are separated by interfollicular tissue derived from the
known collectively as the euplasm); the second is mainly prefollicular tissue. In many species, new follicles are pro-
regulated by genes outside the oocyte, producing pools of duced as the oldest oocytes mature and are ovulated (but
molecules that will subsequently be involved in embryonic see below). As a result, the number of follicles in an ovari-
growth. The vitellarium in a mature insect forms by far the ole may be approximately constant for a species, although
greater part of the ovariole. there is variation between species. Thus Schistocerca com-
The germarium contains prefollicular tissue and the monly has about 20 follicles in each ovariole even in senile
stem line oogonia and their derivatives. The stem line females which have oviposited several times. In Drosophila
oogonia are derived directly from the original germ cells there are usually six follicles per ovariole, while
(section 14.2.13), and, in Drosophila, there are only two or Melophagus has only one follicle in each ovariole at any one
three of these in each ovariole (Spradling, 1993). When time.
they divide, one of the daughter cells remains a functional
stem line cell, while the other becomes a definitive oogo- 13.2.1 Types of ovariole
nium (sometimes called a cystocyte) and develops into an There are two broad categories of ovarioles: panoistic, in
oocyte. Oocytes pass back down the ovariole, enlarging as which there are no special nurse cells, and meroistic, in
they do so, and as each oocyte leaves the germarium it is which nurse cells, or trophocytes, are present. Further,
clothed by the prefollicular tissue which forms the follicu- there are two types of meroistic ovariole: telotrophic, in
lar epithelium. At first this may be two- or three-layered, which all the trophocytes remain in the germarium, and
but ultimately consists of a single layer of cells. Oocyte polytrophic, in which trophocytes are closely associated
growth continues, the follicular epithelium keeping pace with each oocyte and are enclosed within the follicle.
by cell division so that its cells become cuboid or columnar. Trophocytes are sister-cells of the oocytes so that they
In Drosophila, the number of follicle cells surrounding have the same genome, they retain their connections with
each oocyte increases from an initial figure of about 16 to the oocyte because cell division is incomplete, and they
about 1200. During yolk accumulation, growth of the supplement the oocyte in the synthesis of the euplasm. As
oocyte is very rapid, but at this time the follicle cells no a result, the oocytes in meroistic ovarioles have much
longer divide and they become stretched over the oocyte as larger amounts of euplasm than those in panoistic ovari-
a flattened, squamous epithelium. Nuclear division may oles. This has important consequences for the develop-
continue in follicle cells without cell division, so the cells ment of the embryo (14.2.4).
become binucleate or endopolyploid, permitting the high Rapid synthesis of euplasmic constituents can also be
levels of synthetic activity in which these cells are achieved by replication of the chromosomes in the
involved. The functions of follicle cells change during trophocytes without further cell division (endopoly-
oocyte development (Fig. 13.3). At first, they produce ploidy, see below) and by the amplification of genes extra-
some minor yolk proteins and perhaps some of the chromosomally in DNA bodies. This is known to occur in
enzymes that will later be involved in processing the yolk. some species with meroistic ovarioles. An increase in the
OOGENESIS 299
Fig. 13.3. Diagram of the changes in function of cells in the follicle epithelium from just before the start of yolk accumulation
in the oocyte (1) to cell death at the time of ovulation (6). Notice that in (2) the cells are widely separated from each other
allowing the hemolymph to reach the oocyte.
DNA content of these bodies occurs up to the early stages of this type. The prefollicular tissue may be cellular, but
of meiosis, but then they fragment and ultimately dis- sometimes, as in Thermobia (Thysanura), it consists of
appear. small scattered nuclei in a common cytoplasm.
As the oocyte grows, its nucleus increases proportion-
ately in size and is now known as the germinal vesicle. Telotrophic ovarioles Telotrophic ovarioles are character-
Transcription by the nuclear DNA appears to be sup- ized by the presence of trophic tissue as well as oogonia
pressed soon after the beginning of yolk uptake. During and prefollicular tissue in the terminal regions. This
yolk deposition, as the oocyte grows much more rapidly, arrangement is found in Hemiptera and Coleoptera
the germinal vesicle becomes relatively smaller and, finally, Polyphaga. In Hemiptera, each ovariole has only a single
the nuclear membrane breaks down. stem cell that divides to form a cluster of cells which
remain connected to each other by cytoplasmic bridges
Panoistic ovarioles Panoistic ovarioles (Fig. 13.4), which (Fig. 13.5). The most proximal cells are the precursors of
have no specialized nurse cells, are found in the more the oocytes while more distal cells are the trophocytes.
primitive orders of insects, the Thysanura, Odonata, These may divide more frequently than the oocytes so that
Plecoptera, Orthoptera and Isoptera. Amongst the a larger number of trophocytes is produced. The cells all
holometabolous insects, only Siphonaptera have ovarioles remain connected to a central region called the trophic
300 REPRODUCTIVE SYSTEM: FEMALE
primary
oocyte
c)
follicular
vitellarium epithelium
tunica
propria
terminal
oocyte germinal
vesicle
primary
oocyte
interfollicular
pedicel tissue
tunica
externa
oviduct
core. A basically similar phenomenon occurs in the Polytrophic ovarioles As in telotrophic ovarioles, divi-
Polyphaga except that here there are several stem cells in sions of the cells derived from stem cells in polytrophic
an ovariole and each gives rise to columns of cells, the most ovarioles are incomplete so that clusters of cells are
proximal of which is the oocyte (Fig. 13.6). In the more formed. However, unlike telotrophic ovarioles, the
advanced beetle families, the intercellular bridges and cell trophocytes move down the ovariole with their associated
membranes of the trophocytes break down so that the oocyte and become enclosed in the follicle (Fig. 13.7).
oocytes come to be connected with a common trophic Polytrophic ovarioles occur in Dermaptera, Psocoptera,
core. Phthiraptera and throughout the holometabolous orders,
As in other types of ovariole, the oocytes become except for most Coleoptera and the Siphonaptera.
clothed by follicle cells as they leave the germarium, but Divisions of the trophocytes within a cluster are syn-
each oocyte remains connected to the germarium by a chronized by cues (as yet unknown) which pass through
cytoplasmic nutritive cord which extends to the trophic the cytoplasmic bridges. The number of divisions, and so
tissue, elongating as the oocyte passes down the ovariole. the number of trophocytes associated with each oocyte, is
In the beetles this cord is extremely slender, less than 10 characteristic for each species, although in those species
m in diameter. At the time of yolk uptake, the nutritive with larger numbers of trophocytes some variation may
cord finally breaks and the follicle cells form a complete occur. Aedes and Melophagus (Diptera) have seven
layer round the oocyte. trophocytes associated with each oocyte as a result of
Unlike panoistic and polytrophic ovarioles where the three successive cell divisions, Drosophila and Dytiscus
production of new oocytes is a continuous process, divi- (Coleoptera) have 15 trophocytes from four cell divisions,
sion of the germ cells does not continue after oocyte Habrobracon (Hymenoptera) 31, and vespid wasps 63. No
growth begins. As a result, the potential number of oocytes more than six successive cell divisions occur in the
produced by an ovariole is fixed. trophocyte clusters in any insect so the maximum
OOGENESIS 301
trophocytes
trophic
core
prefollicular
nutritive tissue
cord
interfollicular
c) trophocytes oocyte tissue
continue to divide
follicle
epithelium
dying nucleus
trophocyte germinal
vesicle
trophic
core
nutritive
cord
oocyte
number of cells in a cluster is 64 (1 oocyte ⫹ 63 tropho- cytes are pinched off in a separate, but connected, follicle
cytes). Dermaptera are exceptional in having only one from the beginning (Fig. 13.7b).
trophocyte associated with each oocyte, but this results At first the trophocytes are larger than the oocyte, and
from the separation of pairs of cells from larger inter- the trophocyte nuclei enlarge considerably. In Drosophila,
connected groups. the trophocyte nuclei increase in volume about 2000-fold
As each oocyte with its trophocytes leaves the germar- and the chromosomes undergo up to 10 doublings to
ium, the oocyte always occupies a proximal position with produce polytene chromosomes. In the trophocytes of the
respect to the base of the ovariole. All the cells become moth, Antheraea, ploidy levels up to 216 occur. Unlike
enclosed within a common follicular epithelial layer which earlier cell divisions, these mitoses are not synchronized in
soon becomes flattened over the trophocytes, but is the different trophocytes of a follicle. In Drosophila, the
thicker, with cuboid cells, round the oocyte. A fold of fol- trophocytes adjacent to the oocyte have larger nuclei, and
licular epithelium pushes inward separating the oocyte their chromosomes undergo one more replication than the
from the trophocytes except for a median pore. In anterior (distal) trophocytes. These cells subsequently lose
Neuroptera, Coleoptera and Hymenoptera the tropho- their DNA, but the anterior cells do not. In most cases the
302 REPRODUCTIVE SYSTEM: FEMALE
remains of
trophocytes
OOGENESIS 303
13.2.3 Meiosis yolk. Some is associated with the vitellins; most of the
Meiosis begins early in the development of the oocyte, in rest is stored as glycogen. In the terminal oocyte of
most insects, but the meiotic divisions are not completed in Manduca, free carbohydrates contribute about 2% of the
the ovary, and oocytes usually leave the ovarioles in the dry weight.
metaphase of the first maturation division. In Locusta,
meiosis does not proceed beyond the first prophase until 13.2.4.1 Patterns of accumulation in the oocyte
the time of ovulation, and the resumption of meiosis coin- The accumulation of yolk in the oocytes occurs in the
cides with sperm entry in many insects although other lower, proximal part of each ovariole, known as the vitellar-
factors are apparently responsible for the effect. In Locusta, ium, and results in a very rapid increase in size of the
continuation of the process is stimulated by ecdysone from oocyte. In Drosophila, the oocyte volume increases about
the follicle cells to which the oocyte becomes sensitive just 100 000 times during the course of its development.
before chorionogenesis (Lanot et al., 1990), and, in The process of yolk accumulation in insect oocytes is
Drosophila, ovulation triggers the resumption of meiosis commonly called vitellogenesis (see Büning, 1994, for
through some hydration effect (Foe, Odell & Edgar, 1993). example). However, the same term is used to describe the
In viviparous species, such as Hemimerus synthesis of vitellogenin (see Raikhel & Dhadialla, 1992,
(Dermaptera), and in Heteroptera which practice hemo- for example) and it is also used in this sense in other animal
coelic insemination, however, maturation of the oocytes groups. To avoid confusion, synthesis of the specific yolk
and fertilization takes place in the ovary. protein will be referred to as ‘vitellogenin synthesis’, while
‘yolk accumulation’ will be used to describe the accumula-
13.2.4 Yolk tion of yolk in the oocyte.
The euplasm in insect oocytes usually constitutes much In those Lepidoptera, Ephemeroptera and Plecoptera
less than 10% of the total oocyte content. The remaining which do not feed as adults, yolk accumulation is com-
90% or more is yolk, consisting largely of lipids and pro- pleted in the late larva or pupa. In most species, however, a
teins. Lipids often comprise about 40% of the dry weight period of maturation is required in the adult before the
of the terminal oocyte and most of the lipid is stored as tri- oocytes are ready for ovulation. Commonly this period is
acylglycerol (Kawooya & Law, 1988). The protein content only a matter of days, but in cases of adult diapause it may
of the yolk is usually approximately equal to the lipid be very prolonged. Hence it is necessary, in insects, to
content, and 60–90% of yolk proteins are derived from differentiate between becoming adult (that is, having the
vitellogenins. These are proteins manufactured outside outward appearance of an adult with, in most species,
the oocyte, only by females, and with specific uptake wings, and being able to fly) and becoming sexually
mechanisms at the oocyte membrane. Most insects mature.
produce only one or two vitellogenins which range in mol- In many species, yolk accumulation is largely restricted
ecular weight, in different species, from 210 000 to to the oocyte nearest the oviduct in each ovariole (known as
652 000. The vitellogenins are glycolipophosphoproteins the terminal oocyte). The succeeding oocytes remain rela-
in which lipid makes up 7–15% of the total mass and car- tively small until the first is discharged from the ovariole
bohydrates 1–14%. The carbohydrates in the molecule into the oviduct, a process known as ovulation. Hence
are oligosaccharides of mannose. The higher Diptera there is an interval between successive ovulations from any
differ from other insects in producing three to five smaller single ovariole. However, in many Lepidoptera and
yolk proteins varying in molecular weight from 44 000 to Diptera, and in some other insects, yolk accumulation
51 000. When vitellogenins enter the oocyte they often occurs simultaneously in a number of oocytes in each ovar-
undergo some relatively minor modifications and then are iole and fully developed oocytes are stored before oviposi-
known as vitellins. Lipophorin (section 5.2.2.3) may also tion.
constitute a significant part of yolk protein. It makes up Cyclical yolk accumulation is often dependent on
15% of the total protein in the oocyte of Manduca. Other nutrition. This is most obvious in blood-sucking insects,
proteins are present in smaller amounts in addition to free like mosquitoes and triatomine bugs, which take discrete
amino acids. meals with relatively long intervals between them. These
Small amounts of carbohydrate are also present in the insects produce a batch of eggs after each meal and the
304 REPRODUCTIVE SYSTEM: FEMALE
a) b)
75
50 50 1 µl
25
0 0
0 1 2 3 0 20 40 60
blood volume (µl) time after blood meal (hours)
Fig.13.8. Affect of ‘meal’ size on egg production and resorption (Diptera: Aedes). Insects were given blood by enema. (a)
Number of oocytes greater than 200 m long in relation to the amount of blood placed in the midgut (Klowden, 1987). (b)
Effect of amount of blood on resorption. Notice that insects given only 1 l started to accumulate yolk in a similar number of
oocytes to those given 4 l but subsequently more than half the oocytes were resorbed. Oocytes were considered to be
maturing if they were more than 100 m long (after Lea, Briegel & Lea, 1978).
number of eggs produced is proportional to the amount of 20% of soluble protein in the fully developed oocyte. In
blood ingested (Fig. 13.8). addition to these major components, the follicle cells may
Periodicity of yolk deposition also occurs in viviparous contribute other proteins in smaller amounts. Eggs of
and ovoviviparous species perhaps due to the physical con- Blattella, and probably those of other insects, have high
straints imposed by the developing embryos. The vivipar- concentrations of the protein calmodulin in the cortical
ous cockroach, Diploptera, retains its ootheca in a brood sac regions and outside the bounding membranes of yolk
and mechanical stimulation by the ootheca is largely granules. Calmodulin is synthesized in the follicle cells and
responsible for the inhibition of yolk accumulation in the may enter the oocyte through gap junctions (Zhang &
oocytes remaining in the ovarioles (see below). Kunkel, 1994). It probably binds calcium which is
Review: Wheeler, 1996 – effects of nutrition involved in the uptake of vitellogenin and perhaps also in
the ooplasmic transport of yolk vesicles.
13.2.4.2 Yolk proteins
Most yolk protein is synthesized in the fat body inde- Control of vitellogenin synthesis Vitellogenin synthesis
pendently of the ovaries. In addition to vitellogenins and is initiated by juvenile hormone acting directly on the fat
lipophorin, some insects are known to produce smaller body in most insects, but in Diptera juvenile hormone acts
amounts of other yolk proteins in the fat body. The fat indirectly. Here, it causes both the fat body and the resting
body of Aedes aegypti also produces proenzymes that are stage ovaries to acquire competence to respond to other
probably involved in yolk metabolism during embryogene- signals.
sis. These enzymes are sequestered in the oocyte outside The synthesis of juvenile hormone by the corpora
the yolk granules in which the vitellins are stored. Similar allata of the female is regulated by signals from the brain
enzymes are produced by many insects. where relevant information from other tissues is inte-
Follicle cells also contribute proteins to the oocyte. In grated. Synthetic activity may be switched on or off. The
the higher Diptera, they produce the same yolk proteins as signal to initiate juvenile hormone synthesis is generally
the fat body, though in smaller amounts. Follicle-specific related to nutrient or mated status. In locusts, mating and
proteins are known to be produced by the follicle cells of some food odors act via neurosecretory cells in the brain to
several Lepidoptera (van Antwerpen & Law, 1993). In the initiate the synthesis and release of juvenile hormone
silkmoth, Bombyx, one of these proteins constitutes about (Fig. 13.9). Blood-feeding also leads to juvenile hormone
Fig. 13.9. Control of vitellogenin synthesis and yolk accumulation in Locusta. (a) Diagram showing the sequence of events that follow
insemination of the female and the transfer of fertility enhancing substance by the male. Numbers show the sequence of events. Stage 6 is
inferred (see text). (b) Release of juvenile hormone from the corpora allata during the first vitellogenic cycle (stage 3 in a) (data from
Gadot & Applebaum, 1985). (c) Vitellogenin concentration in the hemolymph and rate of uptake by the terminal oocytes (stage 5 in a)
(after Gellissen & Emmerich, 1978). (d) Accumulation of ecdysteroid (mainly ecdysone) in the posterior quarter of the terminal oocyte in
the later stages of yolk accumulation. Ecdysone leads to a resumption of meiosis in the oocyte nucleus (data from Lanot et al., 1987). (e)
Hemolymph titer of adipokinetic hormone during yolk accumulation (stage 7 in a) (data from Moshitsky & Applebaum, 1990).
306 REPRODUCTIVE SYSTEM: FEMALE
synthesis in mosquitoes and in Rhodnius; a high-protein appears in the hemolymph when the juvenile hormone
meal has the same effect in Phormia (Fig. 13.10) (Yin et al., titer declines and the larva spins its cocoon. Vitellogenin
1994). There is also some evidence of a direct component concentration in the hemolymph remains high throughout
of regulation from the ovaries. the pupal period, finally declining in the pharate adult as
Juvenile hormone synthesis is regulated by alla- the oocytes accumulate yolk. In Plodia, ovarian develop-
totropins and allatostatins acting on the corpora allata ment early in the pupal period is correlated with high titers
directly via the neural connection to the brain or via the of ecdysone, but vitellogenin synthesis only proceeds
hemolymph (section 21.4). In the viviparous cockroach, when ecdysteroid titers are low (Shaaya et al., 1993).
Diploptera, small terminal oocytes, between 0.6 and 1.4 Reviews: Hagedorn, 1985 – role of ecdysteroids; Hagedorn,
mm long, enhance the rate of synthesis, but large, fully 1994 – oogenesis in mosquitoes; Koeppe et al., 1985 – role of
developed oocytes have an inhibitory effect which acts on juvenile hormone
the brain via the hemolymph. When an ootheca is present,
it stimulates mechanoreceptors in the brood sac which Accumulation of proteins in the oocyte The oocyte is
inhibit juvenile hormone synthesis via the neural pathway surrounded by the follicle epithelium, but, when the
(Stay et al., 1994). oocyte starts to accumulate vitellogenin, extensive inter-
Although there is a decline in juvenile hormone syn- cellular spaces develop between the follicle cells although
thesis at the end of the first gonotrophic cycle in Locusta, the cells remain in contact with each other through gap
vitellogenin synthesis in this insect is further reduced by junctions (Giorgi et al., 1993). The intercellular spaces
adipokinetic hormone acting directly on the fat body (Fig. permit direct access of the hemolymph to the surface of
13.9). The hemolymph titer of this hormone increases the oocyte and the follicle is said to be patent. Vitellogenin
markedly when the terminal oocytes are large. This effect is taken up selectively from the hemolymph and this is
is produced by a hormone titer only about one tenth of that made possible by specific receptors for vitellogenin on the
required to initiate lipid mobilization in the fat body plasma membrane of the oocyte. The receptors with their
during flight (section 6.2.3) so that its two functions do not bound vitellogenin are taken into the oocyte by endocyto-
conflict (Moshitzky & Applebaum, 1990). Although vitel- sis (Ferenz, 1993). The protein is accumulated and stored
logenin synthesis by the fat body stops, the mRNA respon- in yolk bodies, while the receptors are recycled to the
sible for its synthesis is stored for the next cycle of surface membrane.
synthesis (Glinka et al., 1994). The vitellogenins are changed following their
In the Diptera, synthesis of vitellogenin is regulated by accumulation in the oocyte although, in most insects, the
ecdysone (Fig. 13.10). The prothoracic glands which are changes are small. For example. Rhodnius vitellin contains
the principal source of ecdysone in the immature stages, the same four subunits and has the same molecular weight
are no longer present in adults, and ecdysone is produced as the vitellogenin but has more phospholipids and tri-
by the follicle cells. In the female mosquito, Aedes, acylglycerol (Wang & Davey, 1992). Minor changes to the
ecdysone synthesis is itself regulated by a hormone, egg vitellogenins also occur in Carausius (Giorgi et al., 1993),
development neurosecretory hormone, produced by cells but in Blattella the larger of two subunits comprising the
in the brain. Release of this hormone is triggered by a vitellogenin is cleaved into two, and cleavage of the vitel-
blood meal, but it stimulates the follicle cells to produce logenin also occurs in the boll weevil, Anthonomus
ecdysone only if they have already been rendered compe- (Heilmann, Trewitt & Kumaran, 1993). Proteins from the
tent to respond by juvenile hormone. At the fat body, follicle cells are also modified as they enter the oocyte (Sato
ecdysone is changed to 20-hydroxyecdysone which is the & Yamashita, 1991).
active hormone. Ecdysone, or a precursor, is synthesized The uptake of proteins from the hemolymph is regu-
by the follicle cells in other insects such as the locust (Fig. lated by juvenile hormone. This induces patency (Yin,
13.9d), but here its primary function is the regulation of Zou & Stoffolano, 1989) and also produces changes in the
molting during the embryonic period (section 14.2.10). surface of the oocyte. It does not, however, determine the
In some Lepidoptera, all the oocytes are fully devel- specificity of uptake, at least in Drosophila (Bownes et al.,
oped at eclosion. This is the case, for example, in the 1993). The fact that, in many species, only the terminal
cecropia moth, Hyalophora. In this insect, vitellogenin oocyte in each ovariole accumulates yolk appears to occur
OOGENESIS 307
a) neurosecretory
brain cells
hormone from
midgut endocrine fat body
cells stimulates
vitellogenesis
2
yolk accumulation
corpus juvenile patency
1 allatum hormone ecdysteroid
5 synthesis
protein meal ovary
in midgut
meal
(pmole.h -1.gland pair -1)
rate of accumulation
1 protein
(µg.h-1.ovary-1)
meal
10
release rate
5.0
(mg.ml-1)
uptake
0.5 hemolymph by
5 concentration ovaries 2.5
0 0
60 80 100 120 140 60 80 100 120 140
age (hours) age (hours)
d) ecdysteroids
ovarian ecdysteroids (pg.fly -1)
30 600
hemolymph titer (ng.ml -1)
protein oviposition
meal
20 400
hemolymph
10 titer 200
amount
in ovary
0
60 80 100 120 140
age (hours)
Fig. 13.10. Control of vitellogenin synthesis and yolk accumulation in Phormia. (a) Diagram showing the sequence of events
that follow a high protein meal. Numbers show the sequence of events (based on Yin et al., 1994). (b) Release of juvenile
hormone from the corpora allata during the vitellogenic cycle (stage 5 in a) (after Zou et al., 1989). (c) Vitellogenin
concentration in the hemolymph and rate of uptake by the ovaries (stage 5 in a) (after Zou et al., 1989). (d) Ecdysteroid:
hemolymph titer and amount in the ovaries (after Yin et al., 1990).
308 REPRODUCTIVE SYSTEM: FEMALE
because it produces a factor that inhibits yolk uptake by the The chorion (section 14.1.1) is produced wholly by the
younger follicles. This may act via a local intercellular follicle cells. The various layers are laid down sequentially,
interaction or via the hemolymph. usually by addition to the outer surface, but, in the lamel-
In addition to the selective uptake of vitellogenins, late chorion of Lepidoptera, additional material is added
some non-specific uptake from the hemolymph also to layers already present by the insertion of new sheets of
occurs. As a result of this, substances present in the hemo- fibers into the lamellae. As a result, in Lymantria, the
lymph that are not specifically associated with embryonic lamellae increase in thickness from about 0.04 m when
development may be present in the yolk. first laid down to 0.2 m in the fully developed chorion
Review: Raikhel & Dhadialla, 1992 (Leclerc & Regier, 1993). Subsequently, the fibers which
form the lamellae thicken and ultimately fuse together so
13.2.4.3 Yolk lipids that the lamellae now appear homogeneous rather than
Most of the lipid that accumulates in the oocyte is syn- fibrous. During this phase there is some compaction of the
thesized in the fat body; less than 1% is synthesized by the lamellae and the effect of this is to increase the density of
oocyte. In Manduca, 90% of the lipid is carried to the the chorion, a process known as ‘densification’ (Mazur,
oocyte by low density lipophorins. At the oocyte mem- Regier & Kafatos, 1989). In many eggs, the outlines of the
brane, the lipophorin unloads its lipids and is recycled. individual follicle cells producing the chorion are visible
Most of the remainder of the lipid comes from high on the outside of the completed structure.
density lipophorin which is taken up by the oocyte in Proteins constitute over 90% of the endochorion and
Manduca so that it also contributes to the protein content much of the exochorion when this is present. Many
of the yolk. In Hyalophora, however, apolipoprotein III is different proteins are involved: 19 have been recorded in
recycled and only a very high density lipophorin is taken the endochorion of Drosophila eggs, and 100 or more are
up (section 5.2.2.3). The uptake is receptor mediated. present in the chorion of various Lepidoptera. In Acheta
Much of the phospholipid that accumulates in the oocyte (Orthoptera), Oncopeltus (Hemiptera) and Drosophila,
is also transported by lipophorin (Gondim, Oliveira & most of the proteins are large with molecular weights in
Masuda, 1989). excess of 20 kDa. In the Lepidoptera, by contrast, most are
in the range 10–20 kDa. These proteins include structural
13.2.5 Vitelline envelope and chorionogenesis proteins and enzymes responsible for post-secretion
The follicle cells start to produce the proteins of the changes in the chorion.
vitelline envelope (section 14.1.1) as yolk accumulation Some of the proteins are produced at different times by
nears its end. In Drosophila, it starts to form as a number of the follicle cells. As a result, successive layers of the
discrete plaques which subsequently coalesce, but in some chorion may be chemically different (Fig. 13.11b). Where
other insects it is secreted uniformly over the surface of the marked structural differences occur in different parts of
oocyte from the start. It is possible that, in some insects, the chorion, specific proteins may be produced by
the oocyte also contributes to formation of the envelope different regions of the follicle epithelium. The specific
(Zimowska et al., 1995). In insects with polytrophic ovari- proteins are additional to a population of proteins that
oles, the vitelline envelope is only produced round the provide the basic material of the chorion and which are
oocyte, not round the trophocytes. At about the same time produced by all the follicle cells. For example, the cells
the vitelline envelope is produced, the follicle cells also producing the aeropyle crown of the chorion of Antheraea
produce the ligands responsible for determining the synthesize eight proteins that are not made by any other
extreme anterior and posterior ends of the embryo, and follicle cells and a further 15 proteins that are also pro-
those that determine its dorso-ventral axis (section 14.2.5). duced by cells forming some other specific areas of the
Synthesis of the vitelline envelope in mosquitoes is ini- chorion (Mazur, Regier & Kafatos, 1980). These specific
tiated and maintained by 20-hydroxyecdysone which proteins are produced principally towards the end of
reaches a peak in the hemolymph at this time (Raikhel & chorionogenesis (Fig. 13.11c). This may be true for area-
Lea, 1991). After fertilization, as the egg is laid, the specific proteins in general since they are often concerned
vitelline envelope becomes compacted in a number of with surface structures of the chorion.
insects. The endochorion of many insect eggs contains
OOGENESIS 309
300
50
200
100 25
0 0
0 10 20 30 40 50 0 10 20 30 40 50
time (hours) time (hours)
c) protein synthesis -
spatial variation
100
relative rate of synthesis
75
general protein, aeropyle
50
general protein, flat
Fig. 13.11. Chorionogenesis in a moth (Antheraea). (a) Increase in the weight of the chorion with time (data from Paul &
Kafatos, 1975). (b) Temporal variation in the rates of synthesis of three chorionic proteins (indicated by full, dashed and
dotted lines). These examples were selected to show different patterns of synthesis (after Mazur, Regier & Kafatos, 1980). (c)
Spatial variation in protein synthesis. The general protein is produced by all follicle cells. The specific protein is only
produced in the final stages of chorionogenesis in the follicle cells producing the aeropyle region of the egg. Virtually none is
produced by the other follicle cells (represented here by cells forming a ‘flat’ area of chorion). The specific protein is only
produced in small amount relative to the general protein; in the figure amounts are multiplied by 10 compared with the
general protein (after Mazur, Regier & Kafatos, 1980).
extensive spaces where the outer endochorion is supported microtubules and, if there is more than one, they may be
by pillars (see Fig. 14.3). Where this occurs, the follicle held together by cell junctions or simply twist around each
cells produce a ‘flocculent material’ or ‘filler’ which occu- other, as in Dacus (Mouzaki, Zarani & Margaritis, 1991).
pies the space between the pillars and supports the newly Proteins of the chorion are laid down round the processes.
formed outer endochorion which roofs it (Fig. 13.12). As Late in chorionogenesis the cells producing the processes
the chorion dries, this filler collapses, leaving an airspace. degenerate, leaving pores through the chorion.
Functionally similar material is produced at the surface of The chorion of many insect eggs hardens after it is pro-
the eggs of Antheraea where it forms a mold for the pro- duced though sometimes not until the egg is laid. This is
duction of crowns around the openings of aeropyles. the case in mosquitoes, for example, where the egg hardens
Aeropyles, micropyles and other pores in the chorion and darkens during the day after oviposition. Hardening
are formed by long cellular processes from one, two or results from the formation of cross-links between the
three cells (Fig. 13.13). These processes contain bundles of protein molecules, but these links are produced in different
310 REPRODUCTIVE SYSTEM: FEMALE
a) b)
oocyte oocyte vitelline
envelope
inner
endochorion
follicle cells flocculent
follicle cells material
c) d)
oocyte flocculent material
oocyte drying on to
endochorion
airspace
pillar
follicle cells outer
endochorion
follicle cells
Fig. 13.12. Chorionogenesis. (a)–(d) Diagrammatic representation of the formation of air spaces in the chorion. (a) The
vitelline envelope is complete and the first layers of the inner endochorion (hatched) are being produced. (b) A flocculent
material is produced over most of the surface. In gaps between this material the endochorion starts to form pillars. (c)
Secretion of flocculent material is complete and the outer endochorion starts to form outside it (below in diagram). (d) More
outer endochorion is produced and the flocculent material shrinks, leaving air spaces.
soft
endochorion
Fig. 13.13. Chorionogenesis. Formation of pores in the chorion. Sections through the chorion of Rhodnius at the junction of
the cap with the main shell: (a) the complete chorion; (b) formation of an aeropyle by a process from one of the cells. Notice
also the differential activity of other cells at the junction and lines of weakness where the chorion breaks when the larva
hatches (after Beament, 1946).
OOGENESIS 311
motor output to
spermathecal sperm
muscles
genital
oviduct chamber
egg
micropyles
mechanical
mechanosensory stimulation
input by egg
terminal
ganglion of
CNS
The inability to produce or lay fertile eggs also leads to into the oviduct, where it may be stored temporarily
resorption. Yolk accumulation begins in Schistocerca before oviposition. In species where the external ovariole
before the female mates, but in the absence of mating many sheath contains muscle fibers, these probably assist the
oocytes are resorbed. In this species, mature males movements of the oocyte. The elasticity of the tunica
produce a maturation pheromone and even the presence of propria causes it to fold up after the oocyte is shed and
mature males, without mating taking place, reduces the this pulls the next oocyte down into the terminal posi-
amount of resorption. Lack of suitable oviposition sites tion. The empty follicle epithelium of the first oocyte
causes mosquitoes to resorb terminal oocytes, though usually persists, but it becomes greatly folded and com-
fully-developed eggs are retained, and in parasitic pressed and forms a new plug at the entrance to the
Hymenoptera resorption can occur in the absence of a pedicel. The compressed follicle epithelium is known as a
suitable host. corpus luteum and sometimes the corpora lutea of two or
Juvenile hormone is generally involved in the control of three successive ovulations may be present together
yolk accumulation in the oocytes and the lack of this despite the fact that they break down progressively. In
hormone is associated with resorption, at least when all the Melophagus, only a small relic of the follicle epithelium
developing oocytes are affected. The control mechanism persists as much of the debris from the follicle cells and
involved when only some of the oocytes regress is not trophocytes is passed out of the ovariole when this con-
clear, but it is possible that competition between oocytes tracts after ovulation.
for the available nutrients is involved. In some species, at Sometimes, as in Orthoptera, all the ovarioles ovulate
least, it is clear that resorption is not a direct response to a simultaneously, but in other cases, as in viviparous
lack of vitellogenins in the hemolymph. Diptera, the ovarioles function alternately or in sequence.
Review: Bell & Bohm, 1975 In Lepidoptera, which commonly lay large batches of eggs
although possessing a total of only eight ovarioles, the
oocytes may accumulate in the very long pedicels that join
13.3 OVULATION
the ovarioles to the lateral oviducts until a large number is
The passage of the oocyte into the oviduct, a process present. Similarly in some Diptera and parasitic
known as ovulation, involves the oocyte’s escape from the Hymenoptera, such as Apanteles, large numbers of eggs
follicular epithelium and the breakdown of the epithelial may be stored, in this case in the lateral oviducts, thus
plug at the entrance to the pedicel. In Periplaneta, the enabling the insect to lay a large number of eggs quickly
elasticity of the tunica propria helps to force the oocyte when it finds a suitable oviposition site.
OVIPOSITION 313
It is not clear how ovulation is controlled. Where it is How these insects measure size is not generally under-
followed immediately by oviposition, as in Rhodnius, both stood. Queen honeybees apparently use the forelegs to
ovulation and oviposition may be regulated by the same measure the sizes of the cells in which they are ovipositing.
factors (see below). The parasitic wasp, Trichogramma minutum, lays its eggs in
the eggs of other insects and regulates the number of eggs
it lays (but not their sex) by determining the surface area of
13.4 FERTILIZATION OF THE EGG
the host egg. It does this by measuring the curvature of the
The egg is fertilized as it passes into the genital chamber egg surface, probably determined from the angle between
when a few sperm are released from the spermatheca. The the antennal scape and the head, and the time taken to walk
release of sperm in Schistocerca is in direct response to across the egg from one side to the other (the transit time)
mechanosensory input produced by an egg entering the (Schmidt & Smith, 1989). The mechanism by which the
genital chamber. This input to the terminal abdominal female permits or prevents the release of sperm is not
ganglion results in contractions of muscles which com- known in any of these cases although queen bees have a
press the spermatheca and force sperm out (Fig. 13.15). A valve and pump on the spermathecal duct which presum-
similar mechanism of sperm release occurs in the cricket, ably regulates release.
Teleogryllus. In this case, the egg, on entering the genital Females of some insect species have the capacity to
chamber, presses on the cuticle and stimulates subcut- select for sperm quality from amongst the sperm in the
icular mechanoreceptors. The input from these receptors spermatheca. Males of Drosophila subobscura produce long
inhibits the activity of the oviducal muscles so that the egg and short sperm. Male ejaculate contains a predominance
stops moving, and, at the same time, activates the muscles of the former, but long sperm are stored preferentially in
of the spermathecal duct which squeeze the sperm, tail the female’s spermathecae. They are also released prefer-
first, towards the egg (Sugawara, 1993). In other species, entially from the spermatheca so that most eggs are fertil-
sperm may be forced out of the spermatheca by pulsed ized by long sperm (Bressac & Hauschteck-Jungen, 1996).
increases in hemolymph pressure. There is also evidence that twice-mated females of the
In the some insects, the female clearly has the capacity to moth, Utetheisa ornatrix, use sperm from the larger of two
release or withhold sperm according to environmental cues. males, irrespective of whether she mated first or last with
Male Hymenoptera are haploid, developing from unfertil- the larger insect (LaMunyon & Eisner, 1993).
ized eggs. Queen bees lay male eggs in large cells in the comb Sperm entry to the oocyte is facilitated by the orienta-
and female eggs in smaller cells. Females of some parasitic tion of the egg in the genital chamber where the micro-
Hymenoptera tend to lay haploid, male, eggs in small hosts pyles are aligned opposite the opening of the spermathecal
and diploid, female, eggs in larger hosts. For example, the duct. It is usually stated in the literature that several sperm
ichneumonid wasp, Coccygomimus, lays its eggs in the pupa of penetrate each oocyte and that fertilization is effected by
the wax moth, Galleria. It determines whether or not to fer- only one of the sperm while the rest degenerate. However,
tilize an egg from the size of the cocoon enclosing the host there is increasing evidence that monospermy is also
pupa, but it only differentiates between sizes if the cocoon common (Retnakaran & Percy, 1985)
exhibits some chemical characteristic of the pupa (Sandlan, In a few insects, fertilization occurs while the oocytes
1979). The measurement of size made by the parasitoid is rel- are still in the ovary. This is true of those Cimicoidea
ative so that it tends to lay male eggs in the smaller members which practice hemocoelic insemination, and also occurs
of the host population irrespective of their absolute size in Aspidiotus, a coccid, in which the sperm become
(Godfray, 1994). Amongst the Aphelinidae, which parasitize attached to cells which proliferate in the common oviduct
homopterans, female eggs are laid in host nymphs, but male and then migrate to the pedicels.
eggs are laid if the ovipositor enters a larval parasitoid already
within the host. The parasitoid may be of the same species as 13.5 OVIPOSITION
the egg-laying female, or of a different species (Hunter &
Godfray, 1995). The distinction between parasitized and 13.5.1 Female genitalia: the ovipositor
unparasitized hosts is presumably made on the basis of chem- The gonopore of the female insect is usually situated on or
icals encountered by the ovipositor. behind the eighth or ninth abdominal segment, but the
314 REPRODUCTIVE SYSTEM: FEMALE
Ephemeroptera and Dermaptera are exceptional in having the shaft as in tettigoniids (Fig. 13.16b) or reduced as in
the gonopore behind segment 7. In many orders there are the gryllids. Throughout the Orthoptera the gonangulum
no special structures associated with oviposition, although is fused with the first gonocoxa.
sometimes the terminal segments of the abdomen are long The Hemiptera and Thysanoptera have the gonangu-
and telescopic forming a type of ovipositor (see Fig. 11.1). lum fused with tergum 9, while the gonoplac may
Such structures are found in some Lepidoptera, be present or absent. In Pentatomomorpha and
Coleoptera and Diptera. In Musca, the telescopic section is Cimicomorpha the development of the ovipositor is
formed from segments six to nine and normally, when not related to oviposition habit. If the insect oviposits in plant
in use, it is telescoped within segment five. The sclerites of or animal tissue the valves are sclerotized and lanceolate
the ovipositor are reduced to rods in this species. In others, and the anterior strut of the gonangulum is heavily sclero-
as in tephritids, the tip of the abdomen is hardened and tized. Species laying on leaf surfaces, however, have mem-
forms a sharp point, which enables the insect to insert its branous and flap-like gonapophyses and the anterior strut
eggs in small holes and crevices. of the gonangulum is membranous or absent (Scudder,
An ovipositor of a quite different form, derived from 1959).
the appendages of abdominal segments eight and nine, is In the Hymenoptera, the first gonocoxae are usually
present in Thysanura, some Odonata, Orthoptera, absent (although they may be present in Chalcidoidea) and
Homoptera, Heteroptera, Thysanoptera Terebrantia and the second gonapophyses are united. The first gonapophy-
Hymenoptera. Scudder (1961) has attempted to rational- ses slide on the first by a tongue and groove mechanism
ize the terminology associated with the ovipositor and his (Fig. 13.16c). In the Symphyta and parasitic groups, the
terms will be used together with the more generally used ovipositor retains its original function, but in Aculeata it
terminology of Snodgrass (1935). forms the sting. This does not involve any major
Scudder (1961) believes that Lepisma has a basic form modifications of the basic structure, but the eggs, instead
of ovipositor from which those of other insects can be of passing down the shaft of the ovipositor, are ejected
derived. At the base of the ovipositor on each side are the from the opening of the genital chamber at its base. In
coxae of segments 8 and 9. These are known as the first and Apis, the first gonapophyses are known as the lancets and
second gonocoxae (first and second valvifers of Snodgrass, the fused second gonapophyses as the stylet. This forms an
1935) (Fig. 13.16) and articulating with each of them is a inverted trough, which is enlarged into a basal bulb into
slender process which curves posteriorly. These processes which the reservoir of the poison gland discharges.
are called the first and second gonapophyses (valvulae of Reviews: Mickoleit, 1973 – evolution in Endopterygota; Quicke
Snodgrass, 1935) and, together, they form the shaft of the et al., 1994 – Hymenoptera; Scudder, 1961 – general
ovipositor. In Lepisma (Fig. 13.16a), the second
gonapophyses of the two sides are united, so that the shaft Sensilla on the ovipositor The terminal abdominal seg-
is made up of three elements fitting together to form a tube ments, and the ovipositor, where one is present, have an
down which the eggs pass. At the base of the ovipositor array of mechanoreceptors. Although chemoreception
there is a small sclerite, the gonangulum, which is attached may be an important factor in oviposition, the number of
to the base of the first gonapophysis and articulates with chemoreceptors on the ovipositor is usually very small.
the second gonocoxa and the tergum of segment 9. The Insects receive most chemical information about their
gonangulum probably represents a part of the coxa of oviposition substrates from tarsal or antennal sensilla.
segment 9. It is not differentiated in Petrobius Trichoid mechanoreceptors are generally present and
(Archaeognatha). these may have directional sensitivity (Kalogianni, 1995).
In some Thysanura and in the Pterygota, an additional In addition, small numbers of campaniform sensilla are
process is present on the second gonocoxa. This is the also sometimes reported and may be a usual occurrence.
gonoplac (third valvula of Snodgrass, 1935). It may or may Chemoreceptors have been recorded on the ovipositors of
not be a separate sclerite and may form a sheath round the Orthoptera, Diptera, parasitic Hymenoptera and
gonapophyses. The gonoplacs are well developed in the Lepidoptera. In most cases there are only a few contact
Orthoptera, where they form the dorsal valves of the chemoreceptors. The stemborer moth, Chilo, for example
ovipositor with the second gonapophyses enclosed within has four, and the flour moth, Ephestia, 10 (Anderson &
OVIPOSITION 315
b) tettigoniid
right
second gonoplac
gonocoxa
cut end of left gonoplac
gonoplac
first gonocoxa and
gonangulum fused second
gonapophysis
first
gonapophysis
c) Hymenoptera
tergum 9
(quadrate plate)
gonangulum gonoplac
second gonapophyses
(stylet)
rami of
gonapophyses first gonapophysis
first gonapophysis
(lancet)
Hallberg, 1990). Multiporous, presumed olfactory, sensilla terminal segments of the abdomen are elongated or tele-
have been recorded around the ovipositor in Musca and scopic, may be inserted into crevices. In some cases,
other cyclorrhaphous flies (Merritt & Rice, 1984), and the however, specialized structures are involved in the oviposi-
sunflower moth, Homoeosoma, has 59 on each side tion process. Many Asilidae, for instance, have spine-
(Faucheux, 1991). By contrast, Manduca has no chemo- bearing plates called acanthophorites at the tip of the
receptors associated with the ovipositor, nor has the abdomen. These push the soil aside as the insect inserts the
damsel fly, Sympecma, even though it oviposits in plants tip of its abdomen and oviposits and then, when the
(Gorb, 1994). abdomen is withdrawn, the soil falls back and covers the
eggs. The beetle Ilybius has two finely toothed blades
13.5.2 Mechanisms of oviposition forming an ovipositor. The points of these blades are
In the majority of species which lack an appendicular pushed into the surface of a suitable plant and then worked
ovipositor, eggs are simply deposited on a surface or, if the upwards by a rapid, rhythmic, saw-like action so that a
316 REPRODUCTIVE SYSTEM: FEMALE
a) at rest b) ovipositing
intersegmental
tergum 8 membrane lower part of
gonoplac tergum 9
tergum 7 proctiger
tergum 6 tergum 7
second
sternum 8 gonocoxa
tergum 6
tergum 8
sternum 8 gonapophyses
upper part of
tergum 9
second lower part of
gonocoxa tergum 9 proctiger
gonapophyses gonoplac
Fig. 13.17. Oviposition. Changes in the positions of the basal parts of the ovipositor and the terminal abdominal segments
during oviposition by an ichneumonid wasp (Megarhyssa) (after Snodgrass, 1935). (a) At rest; (b) during oviposition.
tongue of plant tissue is cut away at the sides. An egg is laid membranes between segments 4 and 5, 5 and 6, and 6 and
in the hole beneath the blades and is covered by the tongue 7. The membranes are specialized to permit stretching,
of plant tissue when the blades are withdrawn. having a lamellate endocuticle under a thin epicuticle
Many species with an ovipositor derived from the which is folded at right angles to the long axis of the body.
appendages of segments 8 and 9 penetrate tissues using a As the abdomen lengthens, these folds become smoothed
sliding movement of the valves relative to each other out and the endocuticle stretches. The intersegmental
similar the sting mechanism of Apis. In an ichneumon, the membranes of the male do not stretch to the same extent as
tip of the abdomen is turned down at the start of oviposi- in the mature female, nor do those of the immature female,
tion so that the valves point ventrally instead of posteriorly indicating that some change occurs during maturation.
(Fig. 13.17). The gonapophyses then work their way by The change is controlled by the corpora allata and it is
rapid to and fro movements into the host tissue (or through probable that hydrogen bonding between the protein
the wood in which the host is boring in the case of Rhyssa). chains in the cuticle is reduced by an enzyme from the epi-
The gonoplacs do not enter the wound, but become dermis (Tychsen and Vincent, 1976). The intersegmental
deflected outside it. In this way Rhyssa can bore through 3 muscles are also stretched and they are specialized to
cm of wood in 20 minutes. permit this (see Fig. 10.15).
In grasshoppers (Acrididae), the action of the valves is The extension of the abdomen of grasshoppers may be
quite different, involving an opening and closing move- very considerable. For instance, the abdomen of
ment of the dorsal and ventral valves rather than a sliding Anacridium stretches from 3–5 cm to 10 cm in length and
movement (Fig. 13.19a). These movements are produced Schistocerca can dig to a depth of 14 cm. During digging the
by muscles inserted on to an apodeme at the base of the ventral valves of the ovipositor lever the abdomen down-
valves, and the whole structure is rhythmically protracted wards while the upper valves push soil away and effect the
and retracted. The insect starts by raising the body on the excavation. The pull exerted by the ventral valves is trans-
first two pairs of legs and arching the tip of the abdomen mitted to the abdomen and this results in the extension of
downwards so that it presses more or less vertically on the the intersegmental membranes between segments 4 and 7
ground. The opening movement of the valves scrapes par- (Vincent, 1975). At intervals during digging, the female
ticles of the substratum sideways and upwards and pres- partly withdraws her abdomen and the walls of the hole are
sure is exerted down the abdomen so that the valves slowly smoothed and compacted by small movements of the
dig a hole. As the hole deepens, the abdomen lengthens ovipositor valves together with twisting movements of the
by the unfolding and stretching of the intersegmental abdomen. Even in apparently suitable soil a female
OVIPOSITION 317
frequently abandons a hole and starts to dig again, but (Kalogianni, 1995). The ventral opener muscle is inner-
when a suitable hole has been constructed the process of vated by a motor neuron producing proctolin, and this
oviposition proper begins. Just before an egg is laid, the may also be true of other muscles associated with the
female pumps air into her tracheal system by rapid move- ovipositor valves. It is suggested that octopamine is also
ments of the head and then, with the thoracic spiracles necessary for the normal functioning of the muscle and to
closed, forces the air backwards so that the abdomen maintain the activity of the central pattern generator
becomes turgid. It remains turgid until the egg is laid, then (Belanger & Orchard, 1993).
the head moves forwards again and the pressure is released. The movement of eggs down the oviducts appears, in
Eggs are passed out micropylar end first and the abdomen is Locusta, to result from myogenic activity of the oviducal
slowly withdrawn as more eggs are laid. When all the eggs muscles and a myotropic peptide is present in the hemo-
have been laid, the female fills the upper part of the hole lymph during oviposition. These muscles are also con-
with a frothy plug (Fig. 13.21b) and, finally, after with- trolled neurally, but neural stimulation has the effect of
drawing her abdomen, she scrapes soil over the top of the preventing the backwards movement of eggs. A second
hole with her hind tibiae. The whole process may take about central pattern generator and octopamine from dorsal
two hours, of which egg-laying occupies some 20 minutes. unpaired median (DUM) cells in the subterminal abdomi-
nal ganglion are also involved in integrating these activ-
13.5.3 Control of oviposition ities, but their precise functions are not clear (Facciponte
The readiness to oviposit is influenced by mating. A female & Lange, 1992; Kalogianni & Theophilidis, 1993). A
Bombyx, for example, lays all her eggs within 24 hours of myotropic hormone is also present at maximum titers
mating whereas a virgin female retains most of her eggs for during the period of oviposition of Rhodnius (Davey &
some days. An essentially similar change of behavior Kriger, 1985). It is presumed to have an important role in
occurs in insects belonging to many different orders. It is oviposition, as in Locusta.
induced by peptides or other substances transferred to the
female by the male during sperm transfer (see section 13.5.4 Role of the accessory glands
12.4.2). Under normal conditions, this substance presum- The function of the female accessory glands is generally to
ably causes the female to seek an oviposition site and then, fix eggs in position or protect them from desiccation and
when she receives appropriate stimulation from her predators. Many insects attach their eggs on or close to the
mechano- and chemoreceptors, to begin ovipositing. In larval food source. Lice fix their eggs to hairs; many plant-
Bombyx, the eggs are normally laid close together in a feeding Heteroptera and Lepidoptera lay eggs on the host
single layer; if the trichoid mechanoreceptors on the anal plant. The glue holding the eggs in position comes from
papillae are damaged the eggs are deposited in uneven the female accessory glands. Within the Lepidoptera,
clumps. In the intact insect the information from the hairs insects that drop their eggs from the air, such as the
is relayed to the brain (Fig. 13.18) and from the brain a Hepialidae, lack accessory glands. However, the glands are
command to motor neurons arising in the terminal abdom- well-developed in species that cover their eggs with secre-
inal ganglion leads to contractions of the oviduct so that tion (Hinton, 1981). In Chrysopa (Neuroptera), the eggs
eggs are deposited, and to movements of the abdomen are laid on tall stalks formed from silk produced in the
which result in the eggs being spread regularly over a accessory glands.
surface (Yamaoka and Hirao, 1971, 1977). The accessory glands of the parasitic wasp, Pimpla
In grasshoppers, the activity of the muscles moving the (Hymenoptera), produce hyaluronic acid and a lipopro-
ovipositor valves is regulated by a central pattern gener- tein which coats the egg as it is laid into the host. It is sug-
ator in the terminal abdominal ganglion (Fig. 13.19). In gested that this is a critical factor in preventing
the non-ovipositing insect the activity of the pattern encapsulation by the host hemocytes (Blass & Ruthmann,
generator is inhibited by neural activity from the head 1989) and this may also occur in other parasitic insects
ganglia and the metathoracic ganglion (Thompson, (section 5.3.4).
1986a,b). Sensory input from mechanoreceptors on the The accessory gland secretions of many aquatic insects
ovipositor valves probably helps to maintain and modulate form a gelatinous mass enclosing the eggs. For instance,
the basic rhythm produced by the pattern generator Chironomus dorsalis produces a structure in which the eggs
318 REPRODUCTIVE SYSTEM: FEMALE
brain
muscles of
abdominal
information command segments
to brain from brain
control positioning
5 6 of eggs
1
anal papilla
fertility enhancing
substance from male
3 contact with
substratum
Fig. 13.18. Control of oviposition in the silk moth, (Bombyx). numbers indicate the sequence of events (after Yamaoka &
Hirao, 1971, 1977).
loop backwards and forwards round the circumference of glands. Oothecae are produced by a majority of Blattodea,
the matrix while a pair of fibers, anchoring the mass to the Mantodea and Acridoidea, and by the tortoise beetles,
surface, run through the center (Fig. 13.20b). Other Cassidinae. These structures have precise and character-
species of chironomids and Trichoptera lay their eggs in istic forms which permit respiration by the eggs and the
masses or strands of gelatinous material. escape of the newly hatched larvae while, at the same time,
Female accessory gland secretions have another protecting them from desiccation and from predators.
important function in muscid flies. Here, the secretion Amongst the Blattodea, Blatta, for instance, lays its eggs in
contains proteolytic enzymes and an esterase which have two rows, each of eight eggs, inside a capsule which
two essential roles in fertilization of the egg. They break- becomes tanned as it is formed (Fig. 13.21a). A crest along
down the acrosomal membrane of the sperm, and they the top of the capsule contains cavities connecting via
lead to the digestion of a cap over the micropyle. Whether small pores to the outside and via narrow tubes to the
this also occurs in other insects is not known (Gillott, inside of the ootheca. Immediately below the opening of
1988). each tube, the chorion of an egg is produced into an irregu-
lar lobe containing airspaces which communicate with the
Oothecae Species from several insect groups lay their eggs airspace around the oocyte. Each egg is associated with an
in oothecae formed by secretions of the female accessory air tube in the ootheca.
OVIPOSITION 319
a) retractor opener
muscle muscle dorsal
valve
protractor
muscle
apodeme
inhibition from
head and c)
metathoracic open and protract
ganglia
dorsal opener
dorsal protractor
ventral opener
central
pattern
ventral protractor
generator
motor output
to ovipositor
terminal muscles close and retract
ganglion of
(proctolin)
CNS
dorsal closer
mechanosensory modulates
input from valves output dorsal retractor
ventral closer
ventral retractor
time
Fig. 13.19. Control of oviposition in the locust (Locusta) (mainly after Thompson, 1986a,b). (a) Diagram of the ovipositor
valves and the apodeme to which the dorsal valve hinges. Black spots indicate the origins of muscles on the body wall. Closer
muscles and some accessory muscles are not shown. (b) Diagram of the terminal abdominal ganglion showing some features
of regulation. (c) Pattern of activity in the principal muscles produced by the central pattern generator.
central
fibers
attachment
gelatinous to emergent
1 cm matrix 1 mm structure
320 REPRODUCTIVE SYSTEM: FEMALE
pore
a) Blattodea
air tube
b) Acridoidea
ground
reticular surface
extension of
chorion
1 cm froth
wall of
1 mm ootheca
shell
egg mass
outer chambers
chambers
containing eggs
twig
1 mm 1 mm
Fig. 13.21. Oothecae. (a) Cockroach (Blatta). Left: lateral view of the ootheca; right: transverse section through the crest
showing the passage by which air reaches the eggs (after Wigglesworth & Beament, 1950). (b) Grasshopper (Acrida) (after
Chapman & Robertson, 1958). (c) Tortoise beetle (Basipta). Left: side view; right: view from above showing the chambers
which are produced by secretions of the accessory glands. Each chamber contains one egg (after Muir & Sharp, 1904).
Most Acridoidea lay their eggs in egg pods in the Amongst aquatic insects, all the Hydrophilidae
ground. A pod consists of a mass of eggs held together by a (Coleoptera) produce egg cocoons, or oothecae. These
frothy secretion and is sometimes also enclosed by a layer cocoons are made from silk synthesized in modified ovari-
of the same substance. The hole above the egg-mass is oles. The cocoon of Hydrophilus is molded to the shape of
plugged by more froth (Fig. 13.21b). The number of eggs the abdomen with the aid of the forelegs, then the
in a pod reflects the number of ovarioles in the ovaries and abdomen is withdrawn and the eggs are laid. Finally, the
may vary from one to over 300. The frothy plug permits cocoon is sealed off and remains floating on the surface of
respiration and provides an easy route to the soil surface the water. It is equipped with a silken ‘mast’ about an inch
for the hatching larvae. high, which has a respiratory function (Fig. 13.20a).
Tortoise beetles also produce oothecae. The form and In all these insects, the material from the glands, which
complexity of the ootheca varies from species to species, is initially fluid, is modified as the chemicals from different
but Basipta, for example, attaches its ootheca to the stem of glands mix and come into contact with the outside air. The
its food plant (Fig. 13.21c). The theca is formed of a large process is best understood in Periplaneta. The two acces-
number of lamellae produced from an accessory gland sory glands each consist of a mass of branched tubules
secretion which is compressed into a plate-like form as it is lined with cuticle. The gland cells differ in different parts
extruded between the terminal sclerites of the abdomen. of the glands and in the left gland, which is larger than the
The lamellae form an open cup, occupied by about 30 right, three types are recognizable. They produce the
chambers also formed by the lamellae. An egg is placed in protein from which the ootheca is formed, a -glucoside of
each chamber as it is formed and round the outside of the protocatechuic acid and an oxidase. The right-hand gland
cup the lamellae are plastered firmly together to form a has two types of secretory cell. It secretes a -glucosidase
hard ‘shell’ with looser lamellae outside it. which liberates protocatechuic acid from its -glucoside
REFERENCES 321
when the secretions of the two glands mix in the genital Some insects cover the eggs with material which is not
chamber. The protocatechuic acid is oxidized to a quinone derived from the accessory glands. The heteropteran
by the oxidative enzymes and this tans the protein to Plataspis forms a type of ootheca, laying its eggs in two
produce a cuticle-like structure. A similar process occurs rows and then covering them with hard elongate pellets of
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14 The egg and embryology
[325]
326 THE EGG AND EMBRYOLOGY
surface view
b) Tetrix
section
strut
top of
basal layer strut
vitelline
envelope
yolk
and lepidopteran eggs. Even closely related species may Extensive airspaces are usually present in the chorion
have chorions differing in thickness. In the silkmoths, for adjacent to the oocyte and, in species that lay their eggs in
example, the chorion of Bombyx is about 25 m thick moist environments, these airspaces may extend through
while that of Hyalophora is 55 m thick. These differences the entire thickness of the chorion. This is the case in the
are presumed to have ecological significance. grouse locust, Tetrix (Fig. 14.1b). In the eggs of most
A wax layer is sometimes present on the inside of the species, however, openings through the chorion are
chorion immediately adjacent to the vitelline envelope. restricted, and this limits water loss. For example, in
This has been observed in Drosophila, Rhodnius, grass- Musca, the inner meshwork in the chorion, which provides
hoppers and some Lepidoptera. It may be of general a continuous layer of air all round the developing embryo,
occurrence, at least amongst insects laying their eggs in connects with an outer meshwork by pores (aeropyles)
places where they are subject to desiccation, but it is through an otherwise solid middle layer (Fig. 14.1a). In
difficult to detect and may not always have been recog- many other species, the connections are even more
nized. restricted. For example, in Calliphora (Diptera), the outer
Two anatomically distinct layers, sometimes called the meshwork and aeropyles connecting with the inner mesh-
endochorion and exochorion, are present in the chorion of work are absent over the greater part of the egg, and are
the eggs of some species, but others lack these distinct present only between the hatching lines (Fig. 14.3). Eggs
layers. Even where both are present they are not necessar- of Ocypus (Coleoptera) have an equatorial band of aero-
ily homologous in different species (Hinton, 1969). The pyles connecting with the inner airspaces, Rhodnius eggs
endochorion, which forms the greater part of the chorion have a ring of aeropyles just below the cap (see Fig. 13.13),
in all eggs, is largely proteinaceous, whereas the exochor- and those of Carausius, have a single small pore at which
ion, when it is present, contains some carbohydrate. the reticular inner chorion is exposed at the egg surface.
The innermost layer of the chorion (but outside any The respiratory horns of some Diptera and the Nepidae
wax layer) in many insects is a crystalline layer less than (Hemiptera) serve the same function of connecting the
one micron thick, consisting of proteins stabilized by inner layer of air with the atmosphere outside, while at the
disulfide or dityrosine bonds. In Drosophila, holes in the same time restricting the area through which rapid loss of
crystal lattice are 2–4 nm across, large enough to permit water can occur (Fig. 14.2). This is also true of the micro-
the free movement of oxygen and carbon dioxide. This pylar processes of the Pentatomomorpha which also have a
layer is absent from the eggs of parasitic Hymenoptera. respiratory function (Fig. 14.4a).
THE EGG 327
b)
d)
a) respiratory
horns
central
central meshwork
meshwork
aeropyle
c)
chorion
central
meshwork
inner yolk
meshwork
of chorion
Fig. 14.2. Respiratory horns on the egg of Nepa (Hemiptera) (after Hinton, 1961): (a) whole egg; (b) cross-section of a distal
region of a horn. Arrows indicate the openings of the airspaces to the outside; (c) cross-section of a proximal region of a horn;
(d) longitudinal section of the basal region of a horn where it connects to the chorion round the egg. Notice the continuity of
the air-filled central meshwork of the horn with the inner meshwork that surrounds the egg.
The chorion outside the inner layer of airspaces is shell, produced by the female accessory glands, outward to
sometimes thick and, in Lepidoptera, it is lamellate. The form the projections (Chauvin & Chauvin, 1980).
lamellae are formed from sheets of protein fibers, all the
fibers within a sheet having the same orientation. The Specializations of the chorion
orientation of fibers in successive sheets is rotated so that ESCAPE FROM THE EGG. The first stage larvae of many
they have a helicoidal arrangement through the thickness species escape from the egg by chewing through the
of the chorion. Rotation through 180 ° creates the appear- chorion or by using special egg bursting devices (section
ance of lamellae, in exactly the same way as in chitinous 15.1.1). The chorion of some species, however, has a line of
cuticle (section 16.2.1.1). weakness along which it splits when the larva exerts pres-
The outer surface of the chorion is often sculptured, sure from within. These hatching lines are usually visible
frequently with a basically hexagonal pattern reflecting the from the outside, and sometimes define a cap or operculum.
shapes of the follicle cells which secrete it. Outside this, A cap is present in the eggs of Phasmatodea,
grasshoppers have an additional layer, the extrachorion Embioptera, Cimicomorpha (Heteroptera) and Phthirap-
which differs from the chorion in being produced by gland tera. In Rhodnius, the cap is joined to the rest of the
cells in the oviducts rather than by the follicle cells. chorion by a sealing bar, which is formed from a very thin
The outer covering of the egg of the moth, layer of resistant endochorion (perhaps equivalent to the
Micropteryx, is unusual in consisting of a forest of knobbed crystalline endochorion described above) and a thick
projections. The stalks carrying the knobs are about 50 m amber-colored layer (Fig. 13.13). There are lines of weak-
high and 2–4 m in diameter, and the knobs themselves ness (hatching lines) in the amber layer above and below
are about 10 m in diameter. These are produced in the the sealing bar. Some pentatomid eggs also appear to have
hour following oviposition by exudation from the oocyte a cap, but this has the same structure as the rest of the
itself. The exudate forces the viscous outer layer of the chorion and is not joined to it by a sealing bar.
328 THE EGG AND EMBRYOLOGY
a) b) hatching c)
line
hatching airspaces of
line inner layer
outer
meshwork chorion
yolk
yolk
aeropyle inner
meshwork
Fig. 14.3. Hatching lines in the egg of Calliphora (Diptera) (after Anderson, 1960; Hinton, 1960). (a) Dorsal view of the
whole egg. (b) Cross-section through the middle of the egg. (c) Detail of a section through one of the hatching lines where the
air-filled spaces are back-to-back. Arrows indicate the openings of the airspaces to the outside.
Amongst the Diptera, the eggs of Muscoidea have pyles, but different species of Coreidae have between 4 and
hatching lines in the form of two ridges running longitudi- 60, and pentatomids from 10 to 70. Eggs produced by older
nally along the length of the egg (Fig. 14.3). Along these females of Rhodnius have a reduced number of micropyles
lines, the inner layer of the chorion extends outward so compared with those laid by younger females. There are no
that each ridge contains two inner layers which are back to micropyles in the eggs of species of Cimicoidea which are
back, creating a line along which the chorion is relatively fertilized in the ovary (section 12.3.3.3).
weak. In Drosophila melanogaster, there is a discontinuity in Sometimes the micropylar openings are associated
the endochorion where an operculum meets the body of with aeropyles and are raised above the surface of the egg.
the egg, and, along this line, the two parts are held together This occurs in Pentatomomorpha, and in Oncopeltus each
only by the thin innermost layer of the endochorion and a consists of a cup on a stem (Fig. 14.4a). The micropylar
layer of exochorion. The vitelline envelope is also modified canal passes through the middle of the process and
along this line. It is not certain how important these through the chorion and is surrounded by an open reticu-
devices are as many species, even some Drosophila species, lum enclosing airspaces.
appear to have no weak lines in the chorion. Reviews: Cobben, 1968 – Heteroptera; Margaritis, 1985
yolk
b) Locusta
inner
opening
chorion
micropylar
openings
yolk micropyle
outer
opening
around the egg into which gas from the surrounding water organic acids and other surface active substances is lower
may diffuse. Thus the chorion acts as a plastron (section than that of clean water, and the ease with which a plastron
17.5.2.2), but the effectiveness of a plastron depends on is wetted, and hence ceases to function, is inversely propor-
the area available for gaseous exchange, that is, on the tional to the surface tension. Thus the plastron of insect
extent of the air/water interface. In the eggs of eggs which are laid in organic materials subject to flooding
Lepidoptera and most Heteroptera, Rhodnius, for needs to have a high resistance to wetting if it is to continue
example, the air/water interface is too small to be of functioning in spite of the low surface tension. It must also
significance since it is limited to the openings of the aero- be able to withstand wetting by raindrops which, momen-
pyles. Nevertheless, these eggs may survive some degree of tarily, may exert a pressure approaching 50 kPa. Hence,
flooding by virtue of the fact that they can tolerate a great although eggs in dung and similar situations can rarely be
reduction in their metabolic rate. subject to flooding by more than a few centimeters of
In other insects, the plastron is larger and more water, they possess a plastron capable of withstanding
effective. In Calliphora, where the plastron occurs between flooding by clean water to a much greater depth, and in
the hatching lines, and in Musca, where it extends over the some cases their resistance is greater than that exhibited by
whole egg, normal development continues if the egg is the plastron of some aquatic insects (Hinton, 1969).
immersed in well-aerated water. The respiratory horns of Eggs laid in water, such as those of dragonflies, obtain
many dipteran eggs also form an efficient plastron if the their oxygen from that dissolved in the water. The chorion
eggs are flooded and this is also true in the eggs of Nepidae, in these eggs is generally without any obvious system of
which are essentially terrestrial in their respiration as the spaces and oxygen diffuses through the solid material.
horns normally project above the surface of the water. This is presumably because, in the absence of any need to
The surface tension of water contaminated with restrict water loss, the chorion is relatively porous.
330 THE EGG AND EMBRYOLOGY
500
(mOsmol.l-1 )
b) vitelline envelope
incorporated into
a) outer epicuticle
hydropylar endochorion exochorion
region of outer
serosal cuticle epicuticle
hydropylar
region of inner
serosa epicuticle
serosal
epicuticle
serosal endocuticle
endocuticle
serosa
Fig. 14.7. The hydropyle of a grasshopper. (a) Longitudinal section through the posterior pole of the egg (based on Roonwal,
1954). (b) Detail of the hydropylar serosal cuticle (based on Slifer & Sekhon, 1963).
Water uptake by the eggs of many species is limited to a In most cases, the serosal cells underlying the hydro-
specialized region of the shell called the hydropyle. It may pylar region are larger or more columnar than other cells in
involve a modification of the serosal cuticle, as it does in the serosal epithelium. Even where there are no visible
grasshoppers, or a modification of the chorion itself, as in differences between the serosal cells, they may be func-
some Hemiptera and perhaps also some beetles. In some tionally different, although this is not known to be so.
other insects, as in Notostira and Gryllulus (Orthoptera), There is no evidence, however, that these cells have an
water is absorbed over the whole of the egg and there is no active role in water uptake.
hydropyle. The eggs of whiteflies (Aleyrodidae) have a pedicel at
In grasshoppers, the hydropyle is at the posterior pole one end formed from a hollow extension of the chorion.
of the egg. The inner layer of the serosal epicuticle is The insects attach their eggs to leaves, either by cutting a
deeply invaginated into the serosal endocuticle, and the slit with the ovipositor and inserting the pedicel into the
outer epicuticle is a finely fibrous, proteinaceous material slit or by pushing the pedicel into a stoma. The eggs take
which fills the folds (Fig. 14.7). The serosal endocuticle is up water from the leaf via the pedicel (Byrne, Cohen &
thinner in this region than elsewhere. Draeger, 1990).
By contrast, in eggs of the water scorpion, Nepa, the The eggs of the stick insect, Extatosoma tiaratum, are
hydropyle comprises a fine meshwork within the chorion exceptional in being able to take up water from the atmos-
which is isolated from the surrounding chorion. The phere even at very low vapor pressures. The mechanism of
region, which is normally in the water, provides a direct uptake, which is active, is not known (Yoder & Denlinger,
route through the chorion to the surface of the egg cell. 1992).
Whether the hydropyle is formed from the chorion or Review: Hadley, 1994
the serosal cuticle, the outer part is hydrophilic so that it
readily holds water. In the grasshoppers, the outer serosal
14.2 EMBRYOLOGY
epicuticle performs this function and the thin, folded
inner epicuticle is freely permeable, whereas it is Immediately following fertilization, as the egg is laid, the
impermeable over other parts of the egg. It becomes zygote nucleus divides and the daughter nuclei migrate to
impermeable in species that have an egg diapause, and the the periphery of the egg to form a layer of cells, the blasto-
end of diapause is associated with an increase in perme- derm, surrounding the yolk. Part of this cell layer becomes
ability. thickened to form the germ band from which the embryo
EMBRYOLOGY 333
head
original
ANTERIOR position of appendages
embryo
DORSAL VENTRAL
POSTERIOR
Fig. 14.10. Diagram showing the position of the germ band (stippled), the position of the embryo before blastokinesis (solid
black, showing the protocephalon and gnathal and thoracic appendages), and movement of the embryo at katatrepsis. In all
cases the embryo finally comes to lie on the ventral surface of the egg with its head at the anterior pole. (a) termite
(Kalotermes, Isoptera); (b) Cricket (Acheta, Orthoptera); (c) backswimmer. The embryo first develops on the dorsal side of the
egg and moves to the ventral side (transverse arrow) before reversing its position in the egg (Notonecta, Hemiptera); (d) green
lacewing (Chrysopa, Neuroptera); (e) honeybee (Apis, Hymenoptera).
Lepidoptera, the blastoderm is differentiated into germ sumptive mesoderm and midgut (Fig. 14.12a). The pre-
band and extra-embryonic tissue from the time of its first sumptive stomodeum and proctodeum lie at either end of
appearance, and, in some other insects, such as this. In higher Diptera and some Lepidoptera and
Mallophaga and Apis, the whole blastoderm is thick ini- Hymenoptera, the fate of the different parts of the egg is
tially but subsequently becomes thinner except for the much more precisely determined, but the same general
germ band. arrangement of presumptive areas exists (Fig. 14.12b). In
In eggs containing little cytoplasm, like those of most holometabolous insects, these presumptive areas relate to
insects with panoistic ovarioles, the germ band is a small the development of larval tissues, but, where most or all of
disc or streak of tissue over the posterior end of the egg the adult tissue develops from imaginal discs (section
(Fig. 14.10). In insects with polytrophic ovarioles it is more 15.3.2.2), these areas may also be determined at a very
extensive and, in dipteran eggs, which contain a relatively early stage of embryonic development.
small amount of yolk, the germ band is formed from most
of the blastoderm and there is very little extra-embryonic 14.2.5 Determination of the body axes and
tissue. Where the germ band is short relative to the whole segmentation
egg, embryonic development usually involves the Regulation of blastoderm production and its subsequent
differentiation of additional tissue posteriorly. Where the development into the embryo is most fully understood in
germ band is large, all the parts of the larval body are Drosophila. The features of the longitudinal axis are deter-
represented from the outset. mined by three systems that are maternal in origin (Fig.
The germ band is differentiated into a broad head 14.13). While the oocyte is still in the ovary, the tropho-
region, the protocephalon, and a narrow ‘tail’, the proto- cytes produce a specific mRNA that is transferred to the
corm (Fig. 14.11a) and, in a typical hemimetabolous oocyte and accumulates at the anterior end. Soon after the
insect, the midventral cells of the germ band are the pre- egg is laid, translation of this mRNA occurs to produce a
336 THE EGG AND EMBRYOLOGY
a) b) c)
labrum
eye
antenna
protocephalon
mandible
maxilla
labium
leg 1
protocorm
leg 2
leg 3
pleuropodium
unsegmented
abdomen
abdominal
appendages
Fig. 14.11. Early stages in the development of an insect with a short germ band showing the whole embryo with the
embryonic membranes removed (Ornithacris, Orthoptera).
b) Dacus
embryonic extra-embryonic labial cerebral
ectoderm ectoderm ectoderm ganglion
proctodeum pre-oral
ectoderm
pole cells
posterior stomodeum
midgut
anterior
mesoderm midgut
anterior
midgut
yolk
invaginating
mesoderm
b) 9 hours
posterior pole extra-embryonic
mesoderm midgut cells proctodeum ectoderm
stomodeum
anterior
midgut
embryonic yolk
ectoderm yolk
vitellophages sac
c) 12 hours extra-embryonic
posterior pole ectoderm
mesoderm midgut cells proctodeum
stomodeum
embryonic anterior
ectoderm yolk midgut
vitellophages yolk
sac
14.2.8 Movements of the embryo comes to lie with its head-end towards the posterior pole of
The early embryos of most hemimetabolous orders are the egg. This movement is known as anatrepsis.
small relative to the size of the egg and in many of these Comparable displacements of the embryo occur in
groups the embryo makes extensive movements during Ephemeroptera, Odonata, most Orthoptera and hemipter-
development. In Blattodea, Dermaptera and Isoptera the oid insects.
germ band initially lies on the dorsal surface of the egg Following the period of elongation and development of
near its posterior pole. In most of these insects, as the germ the appendages, the amnion and serosa, which enclose
band lengthens it extends onto the ventral surface and the these embryos, fuse and rupture close to the head. The
head moves to a more posterior position (Fig. 14.10a, embryonic membranes now pull back from the embryo
14.18). In other hemimetabola, the movements are more leaving it exposed on the surface of the yolk (Fig. 14.19e,
marked and the embryo becomes immersed within the 14.20). In species in which the embryo is already on the
yolk (Fig. 14.10b, 14.19d). The posterior end of the germ ventral surface of the egg, it stays where it is, but in species
band is flexed upwards into the yolk, so that the embryo where it has developed on the dorsal side of the egg with its
340 THE EGG AND EMBRYOLOGY
a) b) c)
blastoderm serosa
yolk
amnion
germ amniotic germ amniotic germ amniotic
band fold band cavity band cavity
Fig. 14.16. Development of the amniotic cavity: (a) lateral folds beginning to grow over the germ band; (b) lateral folds meet
beneath the germ band; (c) amnion and serosa separated; embryo immersed in yolk.
Fig. 14.17. Early stage in the invagination of the embryo of 14.2.9 Dorsal closure
Machilis (Thysanura) showing the differentiation of the extra- One effect of katatrepsis in many insects is to reverse the rel-
embryonic membrane into proamnion, with small nuclei, and ative positions of embryo and yolk. At first, the embryo lies
proserosa, with large nuclei (after Johannsen & Butt, 1941). on or in the yolk, but when the movements are completed
the yolk is contained within the embryo. At first, the dorsal
head towards the posterior pole, it now moves round to lie enclosure of the yolk is formed by the extra-embryonic
with its head towards the anterior pole (Figs. 14.10, membranes; later the provisional tissue is replaced by the
14.19f). This movement is known as katatrepsis. The term embryonic ectoderm which grows upwards to form the
blastokinesis is sometimes used synonymously with definitive dorsal closure. As the ectoderm extends, amnion
katatrepsis, but it is also, and preferably, used to refer to all and serosa shrink and become confined to an antero-dorsal
the movements of the embryo within the egg, including region where the serosa finally invaginates into the yolk in
both anatrepsis and katatrepsis. the form of a tube. This is known as the dorsal organ; it is
In holometabolous insects, the embryo elongates and ultimately digested in the midgut (Fig. 14.20a).
differentiates with its head towards the anterior pole of Where no marked katatrepsis occurs, the dorsal
the egg, and the extensive movements which occur in closure is produced by rearrangement of the embryonic
EMBRYOLOGY 341
serosa
chorion
abdomen
blastoderm
legs
protocorm
yolk
protocephalon
germ head
band
gnathal
appendages
antenna
Fig. 14.18. Early stages in the development of an embryo with a short germ band seen from the side. The amnion is not
shown; it covers the outer surface of the embryo (termite, Zootermopsis, Isoptera)
DORSAL VENTRAL
d) POSTERIOR e) f)
serosa
serosa
serosa
abdomen head
gnathal
appendages
thorax abdomen
a) Orthoptera
serosa dorsal organ
(serosa)
serosa
amnion amnion
yolk
ectoderm
amnion
embryo
b) Coleoptera
dorsal organ
(amnion)
ectoderm
serosa serosa
amnion serosa
amnion
c) Lepidoptera
yolk
serosa ectoderm
amnion
amnion serosa
Fig. 14.20. Dorsal closure and the fate of the embryonic membranes. The earliest stages, figures on the left of the diagram,
can be derived from (b) or (c) in Fig. 14.16 (from Imms, 1957). (a) Amnion forms the provisional dorsal closure. Serosa
contracts and is destroyed (Oecanthus, Orthoptera). (b) Amnion forms the provisional dorsal closure. Serosa remains intact
around the outside of the embryo (Leptinotarsa, Coleoptera). (c) Ectoderm forms the dorsal closure. Amnion and serosa
remain intact, enclosing a layer of yolk outside the embryo (Lepidoptera).
membranes even though the embryo itself remains rela- Tenthredinidae so that a layer of yolk is present all round
tively static. In Leptinotarsa (Coleoptera) and other the embryo, held between the amnion and serosa. This pro-
Chrysomelidae, the amnion breaks and grows up inside the vides the first meal for larval Lepidoptera when they hatch.
serosa (Fig. 14.20b). Later it is replaced by the ectoderm Although there is a considerable increase in the area of
while the serosa remains intact round the outside. In the epidermis during dorsal closure, it appears to be pro-
Lepidoptera, Tenthredinidae and Nematocera, amnion duced by changes in the shapes of the epidermal cells, and
and ectoderm grow dorsally together so that the ectoderm not by the addition of more cells.
forms the dorsal closure from the beginning and the
amnion forms a membrane all round the outside (Fig. 14.2.10 Ectodermal structures
14.20c). The serosa is invaginated and destroyed in Appendages The whole outer wall of the embryo repre-
Nematocera, but it persists in Lepidoptera and sents the ectoderm, and the appendages are formed by its
EMBRYOLOGY 343
outgrowth. The labrum develops in front of the sto- whole, occurs partly as a result of cell division and partly
modeum, and the antennal rudiments grow on either side by changes in the shape of the appendages and rearrange-
on the protocephalon (Fig. 14.11c). The protocorm ment of the cells. Four phases of growth are recognizable
becomes segmented and, in the lower orders, each in a grasshopper embryo (Fig. 14.26 center). In the first,
segment extends laterally to form the rudiment of an which lasts up to blastokinesis, the increase in size is rela-
appendage. The anterior appendages in grasshoppers are tively slow and results from an increase in cell number.
first apparent when about 30% of the total incubation Just after blastokinesis, a rapid increase in length occurs
period has elapsed (Fig. 14.11, 14.26). (phase 2) associated with a further increase in cell
Immediately behind the protocephalon are the rudi- numbers. After this, it is probable that no further mitosis
ments of the mandibles, maxillae and labium. The latter occurs in the epidermal cells until apolysis of the second
arises in series with the rest as a pair of limbs that later fuse embryonic cuticle. During this period (phase 3) the
in the midline to form the definitive labium. The append- embryo remains almost constant in length. Once the
ages of the next three segments form the walking legs. cuticle of the first stage larva is produced, no further
These grow longer and become folded and grooved where mitosis occurs and the slow growth before hatching (phase
later the cuticle will become segmented (Fig. 14.11c). 4) is due to changes in the shapes of the cells. Growth at
The abdominal appendages subsequently disappear this time is limited because the embryo occupies the whole
except that in some insects the appendages of segments 8 of the egg, but at the time of hatching a very rapid exten-
and 9 contribute to the ovipositor and those on segment 11 sion occurs due to the flattening of the cuticle (see Fig.
form the cerci. In Orthoptera and some other orders, the 16.22). This final expansion is more marked in the
appendages of the first abdominal segment also persist for appendages than in the body as a whole.
a time. They are known as the pleuropodia and have a In Drosophila, mitosis in the epidermal cells remains
distal area in which the cells become very large. They then relatively synchronized through the sixteenth division
degenerate, becoming torn off when the insect hatches. In which is completed by the time 30% of the developmental
Orthoptera, they probably secrete an enzyme which period has elapsed (for brevity, times are subsequently
digests the serosal endocuticle before hatching. They referred to as ‘x% development’, and see section 14.2.15).
probably serve the same purpose in Belostoma No further mitosis occurs in the epidermis, and growth
(Heteroptera), where they sink into the body so that only results from changes in cell shape and arrangement.
the tip of the appendage projects from a bowl-shaped Amongst holometabolous insects where the imaginal
cavity and they reach their greatest development just appendages develop from imaginal discs, the latter may
before hatching. However, in the cockroach, Diploptera, already be apparent in the embryo. In Drosophila, the discs
the external and lateral membranes of the cells of the pleu- invaginate beneath the surface of the embryonic epidermis
ropodia are associated with large numbers of mitochon- at about 60% development. Initially, the imaginal cells
dria, resembling fluid-transporting tissues. Possibly they remain an integral part of the epidermis, connecting with
are concerned with fluid regulation or osmoregulation in the surface by long, narrow extensions which collectively
the embryo and the fluid surrounding it. form a small placode in the epidermis, but they sub-
The pleuropodia have a specialized function in sequently become completely separated from the surface
Hesperoctenes (Heteroptera). The egg of this insect has no in the peripodial cavities (section 15.3.2.2).
yolk or chorion as it develops within the female parent. Its
pleuropodia grow and fuse together to form a membrane Nervous system The central nervous system arises from
which completely covers the embryo and makes contact ectodermal cells on the ventral side of the embryo.
with the wall of the oviduct to function as a pseudo- Individual cells divide tangentially cutting off large cells
placenta (section 14.3.2.1). called neuroblasts on the inside. This occurs at about 20%
The pleuropodia assume a variety of forms in of development in Drosophila. The number of neuroblasts
Coleoptera, but in Dermaptera, Hymenoptera and is constant in each segment, and is similar between seg-
Lepidoptera they are only ever present as small papillae ments (Fig. 14.21a) and even between species as widely
which soon disappear. different as a grasshopper and Drosophila. Most neuro-
Growth of the appendages, as of the embryo as a blasts divide to form neurons, but one gives rise to glial
344 THE EGG AND EMBRYOLOGY
Other ectodermal structures The tracheal system arises forms a continuous layer on the inside of the eggshell until
as bilateral segmental invaginations of the epidermis the first stage larva hatches. Another very thin cuticle is
which become T-shaped. The arms of the T in adjacent produced by embryos of Acrididae after about 35% of the
segments fuse to form the longitudinal trunks and further developmental period has elapsed (Fig. 14.26). A similar
invaginations from these develop into the finer branches cuticle is present in Phasmatodea and at least some
of the system. Heteroptera and Lepidoptera. Soon after blastokinesis in
Oenocytes (section 16.1.3) are cut off from the epi- insects belonging to the hemimetabolous orders and at
dermis of all the abdominal segments except possibly the least some belonging to the Neuroptera, Trichoptera,
last two. Lepidoptera and Coleoptera, a second embryonic cuticle is
The foregut and hindgut are ectodermal in origin, formed. It is thicker than the first, about 6 m in the
being formed from the stomodeum and proctodeum, grasshopper, Melanoplus, and comprises an epicuticle and
respectively. Their development is considered together a chitinous endocuticle. The first embryonic cuticle
with the midgut. becomes broken up and is no longer visible in the later
The Malpighian tubules arise as evaginations from the stages of embryogenesis. At 75–80% development, the
tip of the proctodeum and so are ectodermal in origin. second embryonic cuticle also separates from the epi-
Early in their development, a large cell becomes apparent dermis and the cuticle of the first stage larva is laid down.
at the tip of each evagination. This cell does not divide, but The second embryonic cuticle, however, remains intact. In
regulates the continuous division of cells close to it so that grasshoppers, it forms the outer covering of the vermi-
the proximo-distal axis of the tubule becomes elongated. form larva (section 15.1.2), serving to hold the appendages
Development begins at 36% of development in Rhodnius close against the body of the insect during hatching.
(Skaer, 1992). Usually only two or three pairs of tubules The Diptera do not have embryonic cuticles, and the
develop in the embryo, but others may be produced during cuticle of the first larval stage starts to form at about 80%
larval development. development as dorsal closure becomes complete.
Review: Manning & Krasnow, 1993 – development of the Cuticle production and molting in the embryo appear
tracheal system in Drosophila to be regulated by ecdysteroids just as in postembryonic
molts. In Locusta and Bombyx, the three major ecdyster-
Embryonic cuticles The first cuticle to be produced oids in the embryo are ecdysone, 20-hydroxyecdysone and
during the embryonic development of many insects is the 2-deoxyecdysone. They are produced in the ovary of the
serosal cuticle which is secreted by the blastoderm and female parent by the follicle cells and are already present in
346 THE EGG AND EMBRYOLOGY
the newly laid egg, but in conjugated, inactive forms. Free the body cavity of insects is called a hemocoel, it is strictly a
ecdysone reaches peak levels when the serosal cuticle, the mixocoel in those insects developing coelomic cavities.
two embryonic cuticles and the first stage larval cuticle are Some of the coelomic sacs, particularly those associated
produced (Fig. 14.26). It is not known if the prothoracic with the antennae, may be quite large and make a
glands of the embryo produce ecdysteroids after they significant contribution to the final cavity.
develop. Juvenile hormone is also present in the embryo, After katatrepsis, when the midgut is formed, the
but its role in the embryonic molts is unclear. mesoderm extends dorsally between the body wall and the
Review: Hoffmann & Lagueux, 1985 gut so that the body cavity also extends until it completely
surrounds the gut.
14.2.11 Mesoderm and body cavities The outer walls of the coelomic sacs form the somatic
The mesoderm is derived from the inner layer of the germ muscles, the dorsal diaphragm, the pericardial cells and
band which forms two lateral strands running the length of the subesophageal body. The latter is found in the
the body and joined across the midline by a thin sheet of Orthoptera, Plecoptera, Isoptera, Ischnocera, Coleoptera
cells. In the lower orders, the lateral strands become seg- and Lepidoptera and consists of a number of large binucle-
mented and the somites separate off from each other, but in ate cells in the body cavity and closely associated with the
Lepidoptera and Hymenoptera the somites remain con- inner end of the stomodeum. The cells become vacuolated
nected together. Amongst the Cyclorrhapha, there is a ten- and usually disappear at about the time of hatching, but in
dency for the mesoderm to remain unsegmented. In Isoptera they persist until the adult stage is reached. It is
Dacus, for example, the strands of mesoderm only become usually assumed that these cells are concerned with
segmented as they differentiate into the definitive struc- nitrogenous excretion, but they may be concerned with
tures. The mesoderm in the protocephalon arises in situ in the breakdown of yolk.
the lower orders, but moves forwards from a postoral posi- The somatic muscles are formed from cells known as
tion in the more advanced groups. myoblasts. These fuse together to form syncytia which are
Coelomic cavities develop as clefts in the somites in progressively enlarged by the incorporation of more
Carausius and Formica (Hymenoptera), but by the meso- myoblasts. The syncytia produce processes resembling
derm rolling up to enclose a cavity in Locusta and Sialis axon growth-cones that move over the inner surface of the
(Fig. 14.23). In the Heteroptera, the coelomic sacs remain epidermis until they reach their attachment points.
open to the epineural sinus, while in Diptera no coelomic The inner walls of the coelomic sacs form the visceral
cavities are formed. muscles. The gonads, fat body and blood cells are also
Where they are most fully developed, a pair of coelomic mesodermal in origin. The heart is formed from special
cavities is present in each segment of the protocorm, while, cells, the cardioblasts, originating from the upper angle of
in the protocephalon, pairs of cavities develop in associa- the coelomic sacs, while the aorta is produced by the
tion with the premandibular and antennal segments. approximation of the median walls of the antennal
Sometimes one or two more pairs are present in front of coelomic sacs on either side.
the antennae. Subsequently, in Orthoptera and Review: Bate, 1993 – muscle development in Drosophila
Coleoptera, the thoracic and abdominal coelomic cavities
become confluent forming a tube on either side. 14.2.12 Alimentary canal
At the same time as the coelom forms, the primary The foregut and hindgut arise early in development as
body cavity develops as a space between the upper surface ectodermal invaginations, the stomodeum and proc-
of the embryo and the yolk. This cavity is called the epi- todeum (Fig. 14.24). These invaginations carry the ante-
neural sinus and, in Orthoptera and Pediculus rior and posterior rudiments of the midgut into the
(Phthiraptera), it is bounded dorsally by a special layer of embryo. These rudiments then extend towards each other
cells forming the yolk cell membrane (Fig. 14.23). forming two longitudinal strands of tissue beneath the
Soon, the walls of the coelomic sacs break down as the yolk and above the visceral mesoderm. From these strands,
mesoderm which forms them differentiates to form midgut tissue spreads out over the surface of the yolk,
muscles and other tissues. As a result, the coelomic cavities eventually completely enclosing it.
and the epineural sinus become confluent. Thus, although Review: Skaer, 1993 – Drosophila
EMBRYOLOGY 347
pleuropodium yolk
ectoderm
hind leg amnion
amniotic developing
cavity nerve cord mesoderm
zygote
nucleus
cleavage
nuclei
central
nervous splanchnic somatic
system mesoderm mesoderm
oogonia or
gonad spermatogonia
Fig. 14.25. Early segregation of the germ cells during embryonic development. The development of all other tissues involves
extensive nuclear division (based on Anderson, 1962).
determination of cells entering the posterior region of the 14.2.14 Metabolic changes
egg as pole cells. Oxygen uptake by the egg increases throughout develop-
In the Nematocera, all the pole cells migrate to form ment as the embryo increases in size, while the respiratory
the germ cells in the gonads, but, in Cyclorrhapha, some quotient, which at first equals one, soon falls to a low level.
are lost during the migration, perhaps becoming vitel- This suggests that, at first, the small carbohydrate reserves
lophages, and only a proportion of them become germ of the egg are used and that fat subsequently becomes the
cells. Some of these migrate through the blastoderm main metabolic substrate. It has been calculated that, in the
before gastrulation, but others do so only during or after egg of a grasshopper, 75% of the oxygen uptake is con-
gastrulation and are carried forwards and invaginated with cerned in the oxidation of fat. The oxidation of lipid is
the proctodeum (Fig. 14.15). The germ cells become advantageous because it produces relatively large quantities
enclosed by the mesoderm and increase in number before of metabolic water compared with carbohydrates and there
they become separated into columns by the ingrowth of is no nitrogenous waste which would be produced if the
the mesoderm. These columns form the germaria of the embryo used its protein reserves for energy metabolism.
ovarioles or the testis follicles. Initially, the RNA present in the egg is derived from the
The mesoderm which forms the gonads is derived female parent. Transcription of new RNA by the zygotic
from several segments, but condenses to form a single nuclei appears to begin in the early stages of cleavage in
structure on each side of the body. The rudiment thickens Coleoptera and Hymenoptera, but in other orders not
ventrally and gives rise to solid strands of cells in which until the syncytial blastoderm or even the blastoderm
cavities appear to form the lateral ducts. The median ducts proper is formed. This is correlated with the fact that, in
arise from ectodermal invaginations. the Coleoptera and Hymenoptera, mitotic cycles are slow
Review: St. Johnston, 1993 – Drosophila relative to those in the other orders, taking 25 minutes or
EMBRYOLOGY 349
cleavage
pole cell
nuclei appear
cellularization of
blastoderm
epidermal cell
division
dorsal closure
imaginal discs
invaginate
larval cuticle
neurogenesis
motor axons
grow
synapses
develop Fig. 14.28. The effect of temperature on the duration of
muscle embryonic development (milkweed bug, Oncopeltus, Hemiptera)
development (from Richards, 1957).
DNA synthesis
the temperature exceeds a certain level, often in the range
ng.embryo -1.h-1
and, even at 80% relative humidity, only 15% of the eggs rous species, such as Sarcophaga, small numbers of rela-
survive to hatching. In Lucilia (Diptera) there is a linear tively large eggs are produced at each ovulation, and in
relationship between the time of development and satura- Musca larvipara only one large egg is produced at a time.
tion deficit. The increased size of the eggs permits the accumulation of
Many eggs have to absorb water before they can com- more nutriment so that the embryo can develop beyond
plete their development. If there is sufficient moisture in the normal hatching stage and larvae are born in a late
the environment to prevent death through desiccation, but stage of development. In Hylemya strigosa, for instance,
not enough for development to continue, the eggs may the larva passes through the first larval stage and molts to
remain quiescent for some time. Under such circum- the second while still in the egg, casting the first stage
stances the eggs of Schistocerca develop to the beginning of cuticle immediately after hatching. In Termitoxenia,
katatrepsis and then remain quiescent and viable for up to development in the uterine egg goes even further. A fully
six weeks. At any time during this period development will developed third stage larva hatches from the egg immedi-
proceed if more water becomes available. ately it is laid. It pupates a few minutes afterwards and the
In some species, the embryonic period is greatly pro- free-living larva never feeds.
longed by an egg diapause. Many insect species overwinter
in embryonic diapause (section 15.6), and, as an extreme 14.3.2 Viviparity
example, the diapause eggs of the brown locust, Locustana, In some insects in which the eggs are retained after
may survive for over three years. Embryonic diapause fertilization, the embryos receive nourishment directly
occurs at different stages of development in different from the parent in addition to, or instead of, that present
species even within one family. For instance, in the family in the yolk. Such insects are regarded as truly viviparous
Acrididae (grasshoppers), it occurs just after blastoderm and some anatomical adaptations are present in the parent
formation in Austroicetes, just before katatrepsis in or egg which facilitate the transfer of nutriment.
Melanoplus femur-rubrum, but not until 80% development Viviparous species commonly produce fewer offspring
in several other species of Melanoplus. than related oviparous species and this may be associated
with a reduction in the number of ovarioles. Thus
14.3 VIVIPARITY
Melophagus and Glossina (Diptera) have only two ovari-
oles on each side, while in the related, oviparous, Musca
14.3.1 Ovoviviparity domestica there are about 70 ovarioles in each ovary.
Many species retain the eggs in the genital tracts until the Similarly amongst the viviparous Dermaptera,
larvae are ready to hatch, hatching occurring just before or Hemimerus has 10–12 ovarioles on each side, but only
as the eggs are laid. All the nourishment for the embryo is about half are functional, and Arixenia has only three
present in the egg and no special nutritional structures are ovarioles on each side.
developed in the eggs or parent. Viviparity of this sort is Sometimes the eggs are retained and development
called ovoviviparity and it differs from normal oviparity occurs in the ovariole, as in Hemimerus, the aphids and
only in the retention of the eggs. Chrysomelidae. In other insects, such as the viviparous
Ovoviviparity occurs spasmodically in various orders Diptera, the vagina is enlarged to form a uterus. In
of insects: Ephemeroptera, Blattodea, Psocoptera, Strepsiptera and a few parthenogenetic Cecidomyiidae the
Homoptera, Thysanoptera, Lepidoptera, Coleoptera and eggs develop in the hemocoel of the parent.
Diptera, being particularly widespread in the last group Elaphothrips tuberculatus is facultatively viviparous.
from which the following examples are drawn. Sometimes Some females lay eggs that develop into females; others are
a species of Musca that is normally oviparous retains its viviparous and produce only males; and others exhibit
eggs and deposits larvae. Some other Diptera, particularly both modes of reproduction. The switch to viviparity
amongst the Tachinidae, are always ovoviviparous. In appears to be related to the quality of the leaves in which
these species, the eggs are retained in the median oviduct the insects are feeding (Crespi, 1989).
which becomes enlarged to form the uterus. Hagan (1951) recognizes three main categories of
Ovoviviparous tachinids produce large numbers of viviparity and his scheme is followed here.
eggs as do many oviparous Diptera, but in other ovovivipa- Review: Hagan, 1951
352 THE EGG AND EMBRYOLOGY
14.3.2.1 Pseudoplacental viviparity broken, the ovariole sheath appears to assume a trophic
Insects exhibiting pseudoplacental viviparity produce eggs function. It thickens and shows obvious signs of metabolic
containing little or no yolk. They are retained by the activity. Extensive gaps develop in the sheath which
female and are presumed to receive nourishment via permit the direct access of hemolymph, and it is probable
embryonic or maternal structures called pseudoplacentae. that the embryo obtains some nutriment from this source.
There is, however, no physiological evidence concerning When the embryo subsequently develops a serosa, this also
the importance of these structures. Viviparous develop- appears to have a trophic function. The oocyte is invaded
ment continues up to the time of hatching, but the larvae by endosymbionts before the ovariole sheath thickens,
are free-living. while the embryo is at an early stage of development. They
In Hemimerus, the fully developed oocyte has no enter through an extensive pore in the blastoderm, and
chorion or yolk, but is retained in the ovariole during accumulate in cells which become mycetocytes. These
embryonic development. It is accompanied by a single cells are differentiated very early in development. The
nurse cell and enclosed by a follicular epithelium one cell possible roles of the endosymbionts in embryonic nutri-
thick. At the beginning of embryonic development, the tion are unknown (Couchman & King, 1980).
follicle epithelium becomes two or three cells thick and at Pseudoplacental viviparity is also known to occur in a
the two ends thickens still more to form the anterior and psocopteran, Archipsocus, in which the serosa is an impor-
posterior maternal pseudoplacentae (Fig. 14.29). As the tant trophic organ, and in the Polyctenidae (Heteroptera)
embryo develops it comes to lie in a cavity (the pseudo- in which first the serosa and then the pleuropodia function
placental cavity) produced by the enlargement of the folli- as pseudoplacentae.
cle, but it becomes connected with the follicle by Review: Blackman, 1987 – aphids
cytoplasmic processes extending out from the cells of the
amnion and, later, from those of the serosa (Fig. 14.29b). Viviparity in Blattodea Cockroaches are anomalous with
Furthermore, some of the embryonic cells form large respect to viviparity, compared to other orders.
trophocytes which come into contact with the anterior Fundamentally, all cockroaches are oviparous, laying their
maternal pseudoplacenta. The follicle epithelium and eggs in an ootheca which is extruded from the genital
pseudoplacentae show signs of breaking down and this is ducts. In some species, like Periplaneta, the ootheca may be
taken to indicate that nutriment is being drawn from them. carried projecting from the genital opening, but it is finally
Later in development, the serosa spreads all round the dropped some time before the eggs hatch. Other species,
embryo and, with the amnion, enlarges anteriorly to form such as Blattella, continue to carry the ootheca externally
the fetal pseudoplacenta (Fig. 14.29c). By this time, dorsal until the time of hatching. Some others extrude the
closure is complete except anteriorly, where the body ootheca, but then withdraw it into the body where it is held
cavity is open to an extra embryonic cavity, the cephalic in a median brood sac extending beneath the rest of the
vesicle. It is presumed that nutriment passes from the reproductive system. In these species, the ootheca may be
pseudoplacenta to the fluid in the cephalic vesicle and then poorly developed and as the eggs increase in size they
circulates into and around the embryo. The embryonic project beyond the ootheca. In most species the increase in
heart is probably functional at this time thus aiding the egg size results only from the absorption of water, but in
circulation. Diploptera, in which the eggs increase in length by five or
Parthenogenetic eggs of aphids also develop in the six times during embryonic development, there is also an
ovarioles. They are much smaller than eggs that are fertil- increase in dry weight, indicating that some nutriment is
ized when these are produced by the same species of aphid, obtained from the parent after ovulation, although the
and they have very little yolk. The oocyte is only briefly mechanism by which they do so is not known.
surrounded by follicle cells and, as it moves down the ovar-
iole, it separates from them. As a result, it does not become 14.3.2.2 Adenotrophic viviparity
surrounded by a vitelline envelope or a chorion since these In adenotrophic viviparity, fully developed eggs with chor-
are normally produced by the follicle cells. At first, nutri- ions are produced and passed to the uterus where they are
ment is received via the nutrient cords as aphids have retained. Embryonic development follows normally,
telotrophic ovarioles, but later, when the nutritive cord is but when the larva hatches it remains in the uterus and is
VIVIPARITY 353
amnion
posterior maternal
pseudoplacenta pseudoplacental
cavity
ovariole
sheath
pedicel
c)
remains of maternal
pseudoplacenta
remains of maternal stomodeum
pseudoplacenta
appendages
amnion serosa body of
embryo
nourished by special maternal glands. Parturition occurs as the choriothete and it is responsible for removing the
when the larva is fully developed and pupation follows chorion and the cuticle of the first stage larva. It undergoes
within a short time, there being no free-living feeding cyclical development, degenerating during the later stages
phase. This type of viviparity only occurs in a few blood- of larval development and starting to regenerate just
sucking Diptera: Glossinidae (tsetse flies), Hippoboscidae, before larviposition, so that it is fully developed by the
Streblidae and Nycteribiidae. time the next larva is ready to hatch. The choriothete
In Glossina, each ovary has only two ovarioles and these adheres to the chorion and, when this is split longitudi-
function in sequence: first one ovariole on the right pro- nally by the larval egg-burster, pulls it off by muscular
duces a mature oocyte, then one on the left, then the action. The chorion becomes folded up against the ventral
second on the right, and so on. Only one fully chorionated wall of the uterus. The cuticle of the first stage larva is
oocyte is produced at a time. It is fertilized in the uterus pulled off in the same way. When the second stage larva
and embryonic development proceeds rapidly, lasting molts, its cuticle is not shed immediately but it is sub-
three or four days at 25 °C. The larva hatches in the uterus, sequently split by the growth of the third stage larva. The
on the ventral wall of which is a small pad of glandular cells cast cuticles are expelled by the female at parturition.
with a cushion of muscle beneath and other muscles The larva feeds in the uterus on the secretion of
running to the ventral body wall. This structure is known specialized accessory glands, known as milk glands. The
354 THE EGG AND EMBRYOLOGY
trophamnion
others. These larvae have well-developed mouthparts, constitution. Hence the unfertilized eggs of most insects
unlike the majority, and they attack larvae of any compet- contain only X-chromosomes as any Y-chromosome must
ing species of parasite which may lay its eggs in the same come from the male. Whether the egg contains one or two
host. These larvae ultimately die without reproducing X-chromosomes, that is, whether it is haploid or diploid,
(Cruz, 1986). depends on the behavior of the chromosomes at meiosis.
The offspring of one egg are usually all of one sex in Sometimes no reduction division occurs, or reduction is
polyembryonic species of Hymenoptera. There are, appar- followed by doubling of the chromosome number so that
ently, exceptions where both sexes are produced, but, in the diploid, XX, composition of the egg is maintained.
such cases, it is not certain that these might not have arisen These eggs will give rise only to females. Eggs which
from two separate eggs. The development of the parasite undergo a normal reduction division and in which no
embryos is synchronized with specific events in the chromosome doubling occurs remain haploid and, if they
development of the host larva suggesting that it is regu- develop at all, become males. Such haploid males are
lated by the host’s endocrine system (Strand, Goodman & characteristic of some insect groups.
Baehrecke, 1991). Parthenogenesis may be classified according to the
In the strepsipteran, Halictoxenos, formation of the behavior of the chromosomes at the maturation division of
‘trophamnion’ does not apparently involve the polar the oocyte:
bodies and additional embryos are derived from the
Haplo-diploidy – A normal reduction division occurs in the
amnion covering the original embryo.
oocyte, fertilized eggs developing into females, unfer-
Review: Ivanova-Kasas, 1972
tilized eggs into males. This is characteristic of
Hymenoptera and some smaller groups.
14.5 PARTHENOGENESIS Apomictic (ameiotic) parthenogenesis – No reduction divi-
Sometimes eggs develop without being fertilized. This sion occurs so that the offspring have the same genetic
phenomenon is known as parthenogenesis. Occasional constitution as the mother and all are female. This is of
parthenogenesis, following from the failure of a female to common occurrence in blattids, aphids, tenthredinids
find a mate, is probably widespread, but a number of insects and curculionids.
use parthenogenesis as a normal means of reproduction. It Automictic (meiotic) – A normal reduction division occurs,
has been recorded from all the insect orders except but is followed by the fusion of two nuclei so that the
Odonata, Dermaptera, Neuroptera and Siphonaptera. diploid number of chromosomes is restored. Often the
The sex of the offspring developing from an unfertil- female pronucleus fuses with the second polar nucleus, or
ized egg is dependent on the sex-determining mechanism two cleavage nuclei may fuse. In Solenobia (Lepidoptera,
of the insect and the behavior of the chromosomes at the Psychidae) two pairs of nuclei fuse after the second cleav-
meiotic division of the oocyte nucleus. In the majority of age division. Moraba (Orthoptera) is exceptional in
insects, the female is homogametic (XX) and the male having a pre-meiotic doubling of the chromosomes fol-
heterogametic (XY or XO), but the Lepidoptera are lowed by a normal division so that the diploid number is
exceptional with the females having the heterogametic restored. This type of parthenogenesis, in which only
PARTHENOGENESIS 357
females are produced, also occurs in phasmids and hermaphrodites are normally self-fertilizing, but can be
coccids. fertilized by the occasional males which arise from unfer-
tilized eggs. Cross-fertilization between the hermaphro-
An alternative classification based on the sex of the
dites does not occur.
offspring produced as a result of parthenogenesis is as
follows:
14.5.2 Thelytoky
Arrhenotoky – Only males are produced. Thelytokous parthenogenesis probably occurs occasionally
Thelytoky – Only females are produced. in many species of insect. For example, in the Orthoptera,
unmated females of Schistocerca live much longer than
Amphitoky – Individuals of either sex may be produced. It
mated females, but lay about the same number of eggs.
is possible, though not proven, that reproduction in the
Nearly all of these start to develop, but only about 25%
tailor ant, Oecophylla, is an example of amphitoky.
hatch and further heavy mortality occurs in the first larval
stage. Thus the viability of unfertilized eggs is much less
14.5.1 Arrhenotoky than that of fertilized eggs, but, nevertheless, Schistocerca
Facultative arrhenotoky, in which the eggs may or may not can develop parthenogenetically for several generations. It
be fertilized, is characteristic of a few groups of insects. It appears that the only eggs to survive are those in which the
occurs throughout the Hymenoptera, in some chromosomes double after meiosis. Unmated cockroaches
Thysanoptera, the Coccidae Iceryini, some Aleyrodidae also live longer than mated females, but produce fewer eggs
and the beetle Micromalthus. In all of these, the unfertil- with poor viability. In Bombyx the tendency for sporadic
ized, haploid eggs, produce males. parthenogenesis varies in different strains.
In the Hymenoptera, the parent female determines In some other insects, thelytoky is a regular occurrence
whether or not an egg is fertilized by controlling the and, in Carausius and some Thysanoptera, males are
release of sperm from the spermatheca as the eggs pass extremely rare, the whole population normally repro-
down the oviduct. The stimuli prompting the female to ducing parthenogenetically. Sometimes, as in some
withhold sperm are largely unknown. Aphidius lays unfer- Psychidae (Lepidoptera) and Coccidae, a parthenogenetic
tilized eggs during the first two or three hours of oviposi- race exists together with a normal bisexual race. Thus,
tion, but then switches to fertilized eggs. Microplitis lays Lecanium (Homoptera) has one race consisting entirely of
more unfertilized than fertilized eggs at 27 °C, but equal females which reproduce apomictically and another race
numbers at 20 °C. Some other factors are discussed in which is bisexual and exhibits facultative thelytoky. In this
section 13.4. case, fertilized eggs may become males or females, while
Two species of Hymenoptera are known to produce unfertilized eggs develop automictically and so produce
haploid males from fertilized eggs. These are the parasitic females. Commonly such races occur in different areas and
wasps, Encarsia pergandiella and Nasonia. In both cases, in the weevil Otiorrhynchus dubius, for instance, a partheno-
the chromosomes contributed by the male are lost genetic race occurs in northern Europe and a bisexual race
immediately after fertilization. In Nasonia, this is con- in central Europe. In general, parthenogenesis occurs more
trolled by an extrachromosomal factor from the male commonly in the higher latitudes than closer to the equator
(Hunter, Nur & Werren, 1993). and, in the genus Otiorrhynchus, 78% of the species occur-
The coccid, Icerya purchasi, is of interest in that, apart ring in Scandinavia reproduce parthenogenetically, while
from a few haploid males, the adult population consists only 28% of those occurring in the Austrian Alps do so.
entirely of hermaphrodites which are diploid with diploid Constant thelytoky occurs in a few Lepidoptera, such
ovaries, but which also have haploid testes. No true females as the psychid Solenobia, raising the question of sex
occur. When the larva giving rise to an hermaphrodite determination as the females of Lepidoptera are hetero-
hatches from the egg, all the cells are diploid, but after a gametic. Thelytoky in these insects may result from the
time haploid nuclei appear in the gonad. They form a core passage of the X chromosome to the polar body at
from which the testis develops surrounded by the ovary. maturation so that only the Y chromosome remains in the
Oocytes undergo a normal reduction division, but the egg; or two polar nuclei may fuse to give a female XO or
spermatocytes, which are already haploid, do not. The XY constitution, while the egg nucleus degenerates.
358 THE EGG AND EMBRYOLOGY
A completely different explanation supposes that the the females; they mate and winter eggs are produced. All
females are homozygous, YY, and so can give rise only to these generations, except for the last, reproduce partheno-
females (Soumalainen, 1962). genetically and consist entirely of females. In some genera,
Thelytoky can result from apomixis or automixis. In such as Terraneura, only one class of sexuparae is pro-
the parasitic wasps of the genus Trichogramma, it is duced and these individuals give birth to both male and
induced by bacteria in the insect (section 4.3.2.2). In the female sexual forms, an instance of amphitoky.
absence of these bacteria, the wasps reproduce sexually Female aphids, which have an XX constitution, are
(Stouthamer & Kamer, 1994). produced apomictically. Males are also diploid, but XO. In
An unusual type of thelytoky, known as gynogenesis, the parthenogenetic production of males, no reduction of
occurs in the form mobilis of Ptinus clavipes (Coleoptera). the autosomes occurs, but one of the X chromosomes is
This form exists only as triploid females which reproduce lost. The production of males is ultimately under environ-
parthenogenetically, but the development of eggs is trig- mental control (see section 15.5).
gered by healthy sperm of P. clavipes or, less successfully, of Spermatogenesis in male aphids is unusual. The two
P. pusillus. spermatocytes produced from each spermatogonium at the
first meiotic division are different; both have the full comple-
14.5.3 Alternation of generations ment of autosomes, but one has an X chromosome, the other
A number of insects combine the advantages of partheno- does not. The cell without an X chromosome degenerates so
genesis with those of bisexual reproduction using an that only those with an X chromosome undergo the second
alternation of generations. This occurs, for instance, in the meiotic division and only one type of sperm is produced.
gall wasps, Cynipidae (Hymenoptera), which are com- Hence the fertilized eggs can only be female (Blackman,
monly bivoltine (having two generations each year), a 1987).
generation of parthenogenetic females alternating with a Aphids reproduce very rapidly, combining the advan-
bisexual generation. Neuroterus lenticularis, for example, tages of parthenogenesis with viviparity and pedogenesis
forms galls on the underside of oak leaves in which the (section 14.6), so that successive generations are tele-
species overwinters. Females emerge in the spring and lay scoped. In the tropics, where conditions are continuously
eggs. The eggs develop into haploid males, or into females favorable, parthenogenesis may continue indefinitely
in which the diploid condition is apparently restored by without the intervention of a sexual generation.
endomitosis at the blastoderm stage. In this way the bisex- An alternation of generations may also occur in
ual generation arises, the insects emerging from catkin Cecidomyiidae.
galls in early summer. After mating, the females of this Review: Sanderson, 1988 – Cynipidae
generation lay eggs that are fertilized and which produce
the parthenogenetically reproducing females of the fol-
14.6 PEDOGENESIS
lowing spring generation.
Aphids have a more complex alternation of generations Sometimes immature insects mature precociously and are
with several parthenogenetic generations occurring able to reproduce. This phenomenon is known as
during the summer (see Fig. 15.37). Sometimes, as in pedogenesis. Most insects reproducing pedogenetically
Aphis fabae, an alternation of host plants also occurs. The are also parthenogenetic and viviparous. Development of
first generation emerges on spindle (Euonymus) in spring the offspring produced pedogenetically usually begins in
from overwintering eggs. It consists entirely of females, the larval insect.
the fundatrices, which may or may not produce wingless The larvae of Miastor (Diptera, Cecidomyidae) and
generations of fundatrigeniae before a winged generation Micromalthus (Coleoptera) give birth to other larvae or,
develops. These migrate to annuals such as beans and occasionally, lay eggs. Pedogenesis occurs in Miastor only
produce wingless virginopara, of which there may be many under very good or poor nutritional conditions. Under
successive generations. Ultimately, the virginopara intermediate nutritional conditions normal adults are pro-
produce the sexuparae, some of which are winged and duced. Young larvae are set free in the body cavity of the
return to the spindle while others are wingless. The former pedogenetic larva and they feed on the maternal tissues,
produce females, the latter winged males which then join eventually escaping through the body wall of the parent.
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15 Postembryonic development
[363]
364 POSTEMBRYONIC DEVELOPMENT
a) grasshopper c) Rhinocoris
ampulla
retractor
muscles hatching
spines
d) mealworm
egg burster
antenna
seta
membrane
egg burster
head
capsule
Fig. 15.1. Hatching devices. (a) Cross-section through the neck membrane of a grasshopper showing the ampullae (after
Bernays, 1972a,b). (b) The head of a first instar larva of a mosquito. The position of the egg-burster is shown from above and
in a diagrammatic vertical section along the line XX (after Marshall, 1938). (c) Embryonic cuticle over the head of a sucking
bug showing the hatching spines. The cuticle is shed as soon as the larva escapes from the egg (Rhinocoris, Heteroptera) (after
Southwood, 1946). (d) Position of the egg-burster spine at the base of a hair (seta) on the eighth abdominal segment of the
first instar mealworm (Tenebrio, Coleoptera) (after van Emden, 1946).
When the egg is enclosed in an ootheca, the larva Special muscles which assist the hatching process are
escapes from this after leaving the egg. In the Blattodea, known to occur in some insects. They break down soon
the ootheca is split open before hatching by the swelling of after hatching (section 10.2.4).
the eggs as they absorb water. The first stage larvae of
grasshoppers, still enclosed in the embryonic cuticle, 15.1.2 Intermediate molt
wriggle through the frothy plug secreted above the eggs In those insects which possess an embryonic cuticle this
(see Fig. 13.21b). The head is thrust forwards through the separates from the underlying epidermis some time before
froth by elongating the abdomen, the tip of which is hatching, but it is not shed, so that the insect hatches as a
pressed against the substrate to give a point of support, pharate first stage larva (section 15.2). The embryonic
while the cervical ampullae are withdrawn. Then, when cuticle is shed during or immediately after hatching in a
elongation is complete, the cervical ampullae are expanded process commonly known as the intermediate molt. As the
to give a purchase while the abdomen is drawn up. By larva of Cimex or a louse emerges from the egg, it swallows
repeating this cycle the larva tunnels its way to the soil air and, by further pumping, splits the embryonic cuticle
surface following the line of least resistance offered by the over the head. The cuticle is shed as the larva continues to
soft plug. hatch because, in Heteroptera, it is attached inside the
LARVAL DEVELOPMENT 365
chorion at two or three places (Sikes and Wigglesworth, insects, Aedes eggs hatch when immersed in deoxygen-
1931). ated water, the lower the oxygen tension the greater the
The intermediate molt in acridids begins as the newly percentage hatching, but responsiveness varies with age.
hatched larva reaches the surface of the soil. Ecdysis The larvae are most sensitive soon after development is
behavior is triggered by the lack of all-round contact with complete and will then hatch even in aerated water, but if
the substrate which the larva has experienced up to that they are not wetted for some time they will only hatch at
time. The larva swallows air, increasing its volume by very low oxygen tensions. Low oxygen tension is per-
about 25%, and, as it does so, waves of shortening and ceived by a sensory center in the head or thorax and
lengthening pass along the body of the larva causing it to maximum sensitivity coincides with a period of
move forwards within the intact embryonic cuticle. It maximum activity of the central nervous system as indi-
maintains its forward position inside the embryonic cuticle cated by the concentration of acetylcholine. Low oxygen
by backwardly directed spines on the abdominal sternites. tension has completely the opposite effect on the hatch-
As a result of these movements the embryonic cuticle is ing of Agabus (Coleoptera) larvae, which only occurs in
pulled taut over the head and thorax, eventually splitting oxygenated water. Some species of Lestes (Odonata) lay
mid-dorsally. The first stage larval cuticle expands so that their eggs above the water. Fully formed larvae hatch
the insect swells out of the embryonic cuticle, which is when they are wetted.
worked backwards. It is held at the tip of the abdomen by In other species, hatching at a particular time of day
two spiny knobs, called brustia, at the bases of the cerci so results from the entrainment of activity to the cycle of
that the hind legs can be withdrawn and then it is finally changing light or temperature over the previous days.
kicked off by the hind legs. Unhatched larvae of the pink bollworm moth,
Pectinophora gossypiella, for example, are entrained to the
15.1.3 Hatching stimuli light cycle in the days before hatching so that they hatch at
The stimuli that promote hatching are largely unknown dawn (Saunders, 1982). They hatch at the appropriate
and, in many cases, insects appear to hatch whenever they time of day even if they are in continuous light for the last
reach the appropriate stage of development. Even in these day of development. Similarly, the hatching of larval
instances, however, it is possible that some external stimu- Schistocerca gregaria at dawn is not an immediate response
lus influences hatching. to the changing temperature of the surrounding soil, but
Suitable temperatures are necessary for any insect to results from an entrainment of activity to the 24-hour
hatch and there is a threshold temperature below which cycle of temperature changes during the last days of
hatching does not occur. This temperature varies from embryonic development (Fig. 15.2b).
species to species, but is about 8 °C for Cimex, 13 °C for
Oncopeltus and 20 °C for Schistocerca. It is independent
15.2 LARVAL DEVELOPMENT
of the threshold temperature for full embryonic develop-
ment, which may be either higher, as in Cimex (13 °C), or Post-embryonic development is divided into a series of
lower, as in Schistocerca (about 15 °C). The failure of stages, each separated from the next by a molt. The form
fully formed larvae to hatch at low temperatures is that the insect assumes between molts is known as an
related to inactivity. Newly hatched Schistocerca larvae, instar, that which follows hatching or the intermediate
for instance, are not normally active below about 17 °C molt being the first instar, which later molts to the second
and their activity remains sluggish below 24 °C, and instar, and so on until at a final molt the adult or imago
Cimex is not normally active below 11 °C. Further, tem- emerges. No further molts occur once the insect is adult
peratures must be sufficiently high for the enzyme except in Apterygota and non-insect hexapod groups. The
digesting the serosal cuticle to function efficiently (see periods between molts are called stages, or stadia – for
above). example, first larval stage, second larval stage, and so on –
If temperature is suitable and the larva is fully although the term instar is commonly used to refer to this
formed, hatching may be induced by specific environ- period as well as to the form of the insect during the
mental stimuli. For example, larvae of the stem-boring period.
moth, Chilo partellus, hatch just after dawn in response to During larval development there is usually no marked
the high light intensity (Fig. 15.2a). Amongst aquatic change in body form, each successive instar being similar
366 POSTEMBRYONIC DEVELOPMENT
hatching (%)
above each graph. In continuous light (top
left) the insects hatched over an extended 50
period with a peak after about 100 hours of egg
incubation. ‘Lights on’ after about 94 hours of 25
incubation stimulated hatching (bottom left),
0
darkness after this delayed it (right-hand
graphs). In all cases, eggs were maintained at a light
constant temperature of 30 °C with 12 h 100
light :12 h dark cycles up to the time of the
75
hatching (%)
experiment (based on Chapman et al., 1983).
(b) Entrainment to a temperature cycle
50
leading to hatching by larvae of the desert
locust, Schistocerca gregaria. Insects in the 25
upper panel experienced cycling temperatures
0
throughout life. Insects in the lower panel
90 100 110 120 90 100 110 120
experienced cycling temperatures up to the time (hours) time (hours)
beginning of the experiment (time 0 in figure),
but then were maintained at 33 °C. They
hatched at the same time as insects b) Schistocerca
experiencing cycling temperatures despite the temperature 33 28 33 28
fact that they were experiencing a constant 15
temperature. The eggs were in constant
number hatching
temperature 33 33 33 33
15
temperature
number hatching
10
0
0 12 24 36 48
time (hours)
LARVAL DEVELOPMENT 367
first instar second instar third instar Fig. 15.3. Successive stages in the
postembryonic development of a
hemimetabolous insect. The
horizontal line under each stage
represents 0.5 mm (Cyllecoris,
pronotum forewing
pad Heteroptera) (after Southwood &
mesonotum
hindwing Leston, 1959).
metanotum pad
abdomen
pronotum
scutellum
(mesonotum)
forewing
to the one preceding it, but the degree of change from last grows bigger and the genitalia develop progressively.
instar larva to adult varies considerably and may be very Adults and larvae live in the same habitat.
marked. This change is called metamorphosis (Snodgrass, In hemimetabolous insects, the larva hatches in a form
1954; Wigglesworth, 1965). In morphological terms, which generally resembles the adult except for its small
Snodgrass (1954) relates metamorphosis to the loss of size and lack of wings and genitalia (Fig. 15.3), but, in
adaptive features peculiar to the larva, and the extent of addition, usually with some other features which are
change occurring as a reflection of the degree of ecological characteristic of the larva but which are not present in the
separation of the larva from the adult. It can also be adult. At the final molt these features are lost. The
defined in physiological terms as the change which accom- Orthoptera, Isoptera, Hemiptera are commonly regarded
panies a molt in the absence of juvenile hormone. The as hemimetabolous. Snodgrass (1954) calls these groups
term metamorphosis is sometimes applied to all the ametabolous or paurometabolous (that is, with a very slight
changes occurring in the life history, from egg to adult (see metamorphosis), but a quantitative analysis of growth
e.g. Imms, 1957), but it is better not to use it in this wide changes shows a gradual transformation through the larval
sense. instars and a sharp discontinuity at the molt from larva to
The insects can be grouped in three categories, adult. This discontinuity applies not only to typical adult
ametabolous, hemimetabolous or holometabolous, accord- features such as the wings and genitalia, but to other fea-
ing to the extent of the change at metamorphosis. tures that are not regarded as typically adult. In Rhodnius,
Ametabolous insects have no metamorphosis, the adult the larval cuticle with its stellate folds and abundant
form resulting from a progressive increase in size of the plaques bearing sensilla is replaced by the adult cuticle,
larval form. This is characteristic of the Apterygota and which has transverse folds, a few sensilla and no plaques
hexapods other than insects in which the larva hatches in a (section 15.3.1).
form essentially like the adult apart from its small size and The Plecoptera, Ephemeroptera and Odonata have
lack of development of genitalia. At each molt the larva aquatic larvae and their specific larval adaptations are
368 POSTEMBRYONIC DEVELOPMENT
wings
wing pad
gills
caudal
filaments
caudal
filaments
much more marked than in the previous groups. Hence though they are phylogenetically far removed from the
these forms undergo a more conspicuous metamorphosis majority of holometabolous insects.
involving, among other things, loss of the gills (Fig. 15.4). In whiteflies (Aleyrodidae), the final larval stage feeds
The general body form, nevertheless, resembles that of the for a short period but then has an extended non-feeding
adult and these insects are also regarded as hemimeta- period during which the pharate adult develops. This
bolous. stage is commonly known as a pupa (Byrne & Bellows,
In holometabolous insects, the larvae are usually quite 1991) and some texts refer to whitefly development as
unlike the adult and a pupal stage is present between the holometabolous, although there is really no resemblance to
last larval stage and the adult (Fig. 15.5). The pupa is the holometabolous development in other groups.
characteristic of holometabolous development, which The term ‘molt’, as commonly used, includes two dis-
occurs in all the Neuroptera, Trichoptera, Lepidoptera, tinct processes: apolysis, the separation of the epidermis
Coleoptera, Hymenoptera, Diptera and Siphonaptera. from the existing cuticle; and ecdysis, the casting of the old
Amongst the insect groups that typically have a hemi- cuticle after the production of a new one. In the interval
metabolous development, a few have life histories some- between apolysis and ecdysis the insect is said to be
what analogous to those of holometabolous insects. pharate. During this time the cuticle of one developmental
Hemiptera have a typical hemimetabolous development, stage conceals the presence of the next. In most hemimeta-
but in Thysanoptera, which are phylogenetically close to bolous insects and holometabolous larval stages, the
Hemiptera, the last two larval stages do not feed, and the pharate period is relatively short (Fig. 15.6a), but it is often
final stage, which is often called a pupa, is sometimes extended at the larval/pupal molt and pupal/adult molt
enclosed in a cocoon. Both these stages have external wing (eclosion) (Fig. 15.6b) and sometimes may be very long. It
pads, but the earlier larval stages have none; instead, some is most important that this pharate stage is appreciated,
development of the wings occurs internally. Within the especially in relation to the physiology and behavior of
Hemiptera, the last two larval stages of male scale insects insects.
(Coccoidea) also do not feed. These insects clearly have a Some difficulties in terminology arise because of the
life history that can be regarded as holometabolous even pharate period. The terminology usually applied to
LARVAL DEVELOPMENT 369
last instar within the pupal cuticle, so that, although they outwardly
dorsal larva abdominal
process process appear to be pupae, they are, in fact, adults.
stemmata In practice, the pharate stage is not always readily
recognizable and the more usual terminology, with each
stage extending from ecdysis to ecdysis, has been retained
in this book, but with reference to the pharate condition
where it is obviously important.
biting thoracic Review: Sehnal, 1985
mouthparts legs prolegs
a) hemimetabolous
insect
b) holometabolous pharate
adult
insect
Fig. 15.6. Diagram showing the visible stages of development and the times of apolysis and ecdysis, defining the pharate
periods (hatched), in: (a) a hemimetabolous insect; (b) a holometabolous insect; (c) a cyclorrhaphan fly in which the pupa is
always concealed within the puparium.
larvae of Lepidoptera, Mecoptera and Tenthredinidae are sis, but sometimes successive larval instars have
of the polypod type. quite different forms. Development which includes
The third basic form is the apodous larva, which has no such marked differences is termed heteromorphosis.
legs and is very poorly sclerotized. Several different forms [Hypermetamorphosis is sometimes used for this type of
can be recognized according to the degree of sclerotization development, but this implies the use of the term meta-
of the head capsule: morphosis to refer to change of form throughout the life
history rather than restricting it to the larva/adult trans-
1 Eucephalous – with a well-sclerotized head capsule formation.] Heteromorphosis is common in predaceous
(Fig. 15.7d). Found in Nematocera, Buprestidae, and parasitic insects in which a change in habit occurs
Cerambycidae and Aculeata. during the course of larval development. Two types of
2 Hemicephalous – with a reduced head capsule which heteromorphosis occur, one in which the eggs are laid in
can be retracted within the thorax (Fig. 15.7e). Found the open and the first stage larva searches for the host, and
in Tipulidae and orthorrhaphous Brachycera. a second in which the eggs are laid in or on the host.
3 Acephalous – without a head capsule (Fig. 15.7f). In the first type, the first stage larva is an active cam-
Characteristic of Cyclorrhapha. podeiform larva (Fig. 15.8a). In Strepsiptera, this larva
attaches itself to a host, often a bee or a sucking bug, when
15.2.2 Heteromorphosis the latter visits a flower in which the larva is lurking.
In most insects, development proceeds through a series of Subsequently, it becomes an internal parasite and loses all
essentially similar larval forms leading up to metamorpho- trace of legs, while developing a series of dorsal projections
LARVAL DEVELOPMENT 371
d) eucephalous
f) acephalous
which increase its absorptive area. Later, in the sixth segmented abdomen and various tail appendages (Fig.
and seventh stages it develops a cephalothorax. A 15.8c). These larvae hatch from eggs which contain very
basically similar life history with an active first stage little yolk and some authorities regard them as embryos
larva followed by inactive parasitic stages occurs in which hatch precociously (Chen, 1946), but others believe
Mantispidae (Neuroptera), Meloidae and some them to be specialized forms adapted to their environ-
Staphylinidae (Coleoptera), Acroceridae, Bombyliidae and ment (Snodgrass, 1954).
Nemestrinidae (Diptera), Perilampidae and Eucharidae
(Hymenoptera) and Epipyropidae (Lepidoptera). The 15.2.3 Numbers of instars
first stage larvae of Meloidae and Strepsiptera are some- Primitive insects usually have more larval instars than
times called triungulins because, in some species, they advanced species. Thus Ephemeroptera molt as many as 40
have three pretarsal claws (Clausen, 1940; Snodgrass, times, and cockroaches often have 10 molts. In contrast,
1954). most hemipteroid insects and endopterygotes have five or
The second type of heteromorphosis occurs in some fewer larval stages (Table 15.1). Even within a group of
endoparasitic Diptera and Hymenoptera. Amongst the related insects there is variation. Amongst the grass-
parasitic Hymenoptera exhibiting this type of develop- hoppers, Acridoidea, the Pyrgomorphidae have five or
ment, the first stage larva is known as a protopod larva. It more larval instars while the Gomphocerinae, which are
has many different forms in different species and is often also usually smaller, have four.
quite unlike a normal insect (see Fig. 15.8b,c; and Despite these generalizations, the number of larval
Clausen, 1940). The first stage larva of the braconid, stages through which a species passes is not absolutely con-
Helorimorpha, for instance, has a big head, a small unseg- stant. In the Orthoptera, the female, which is often bigger
mented body and a tapering tail (Fig. 15.8b). The third than the male, commonly has an extra larval stage, and
stage larva, on the other hand, is a fairly typical eucephal- larvae hatching from small eggs grow slowly and have an
ous hymenopteran larva. In the Platygasteridae, the first additional stage. The red locust, Nomadacris, may have six,
stage larva is even more specialized with an anterior seven, or occasionally eight larval instars depending on its
cephalothorax bearing rudimentary appendages, a environment and that of the parents. In Plusia and some
372 POSTEMBRYONIC DEVELOPMENT
SEVENTH INSTAR
LARVA
absorptive
processes
b) Helorimorpha c) Platygaster
mandible antenna
mandible
cephalothorax
prothoracic
LATE STAGE appendage
LARVA
other Lepidoptera, larvae reared in isolation may pass steadily throughout a stage of development and then falls
through five, six or seven instars, while nearly all of those slightly at the time of molting due to the loss of the cuticle
reared in a crowd have only five. At least amongst the and some loss of water that is not replaced because the
Lepidoptera, much larger numbers of molts may occur if insect is not feeding. Following the molt, the weight
the insect has a poor food supply, and the larva of the clothes rapidly increases above its previous level. Expressed in
moth, Tineola, is recorded as molting as many as 40 times. terms of the increase in absolute weight, the growth rate
Not all insects have this flexibility, and in most Hemiptera (increase in weight per unit time) is usually greater in the
and cyclorrhaphous Diptera and many Hymenoptera and later stages, but the relative growth rate (the increase in
Coleoptera, the number of instars is constant. weight relative to existing weight in a defined period of
time – often expressed as mg mg⫺1 day⫺1) normally
15.2.4 Growth decreases as the organism increases in size (Fig. 15.9a)
15.2.4.1 Weight (Slansky & Scriber, 1985). In some aquatic insects, there is
There is a progressive increase in weight throughout the no decrease in weight before a molt, but, conversely, there
larval stages (Fig. 15.9). Typically, the weight increases is a sharp increase due to the absorption of water, either
LARVAL DEVELOPMENT 373
Table 15.1. Numbers of larval stages in different orders of The final weight of the adult insect often varies accord-
insects. The commonly occurring numbers are given. Numbers ing to the conditions under which the larva develops. Rapid
outside this range may occur under some conditions development at high temperatures results in adults that are
relatively light in weight. Crowding, possibly through its
Order Common name Number of larval stages effect on the rate of development, also influences adult size,
insects from crowded conditions being smaller than others
Archaeognatha 10–14
reared in isolation. For example, in one experiment on
Thysanura Bristletails 29–14
Locusta, adult females from larvae reared in isolation
Ephemeroptera Mayflies 20–40 weighed 1.5 g, while others from larvae reared in crowds
Blattodea Cockroaches 26–10 weighed only 1.2 g. Where isolation is correlated with the
production of an extra larval instar, the difference in weight
Mantodea Mantids 25–9
may be even more marked. Finally, adult weight may be
Grylloblattodea Rock crawlers 28
influenced by the food on which the larva is nourished. This
Orthoptera Crickets 25–11 is particularly well illustrated in phytophagous insects, such
Phasmida Stick insects 28–12 as the grasshopper Melanoplus sanguinipes in which the
weight of females varies from 140 mg to 320 mg, depending
Isoptera Termites 25–11
on the food available to the larvae. However, insects in which
Dermaptera Earwigs 24–6
the timing of metamorphosis is determined by size (see
Embioptera Webspinners 24–7 below) are much less variable in size as adults.
Plecoptera Stoneflies 22–23
15.2.4.2 Increase in size of the cuticle
Hemiptera Bugs 23–5
Fully sclerotized cuticle does not expand, so growth of scle-
Thysanoptera Thrips 25–6
rotized parts only occurs when an insect molts and a new, soft
Psocoptera Book lice 26 cuticle is produced and expanded. Consequently, hard parts
Phthiraptera Lice 23–4 increase in size in a series of steps (Fig. 15.9b). Membranous
regions can expand, however, by the pulling out of folds.
Neuroptera Lacewings 23–5
Thus a structure with a wholly membranous cuticle, or one,
Mecoptera Scorpion flies 24
such as the abdomen of Locusta, in which the membranes are
Siphonaptera Fleas 23 extensible, may grow continuously. Other regions in which
Diptera Flies 23–6 there is rather less membrane show an intermediate type of
growth with some extension occurring in the course of each
Trichoptera Caddis flies 25–7
stage together with a marked increase at each molt.
Lepidoptera Butterflies 25–6
In many hemimetabolous and ametabolous insects, the
Coleoptera Beetles 23–5 number of annuli in the antennal flagellum increases during
Hymenoptera Bees 23–6 postembryonic life. Thus, the first instar larva of
Dociostaurus (Orthoptera) has antennae with 13 annuli,
while in the adult there are 25. In annulated antennae new
through the cuticle or via the alimentary canal (Fig. annuli are added basally by division of the most proximal
15.9c). annulus of the flagellum known as the meriston. In
In blood-sucking insects, such as Rhodnius, which feeds orthopteroid insects and Odonata some of the annuli adja-
only once during each larval stage, the pattern of growth is cent to the meriston, and derived from it, may also divide.
different. During the non-feeding period of each stage They are known as meristal annuli. At each molt in
there is a slow, steady loss in weight due to water loss and Periplaneta (Blattodea) the meriston divides to produce
respiration, but feeding is accompanied by a sharp increase 4–14 new annuli and each meristal annulus may divide once.
in weight followed by a fairly rapid fall as water is elimi- Where the cerci are segmented, as in Blattodea and
nated. There is, of course, a net increase in weight from Mantodea, they increase in size at successive molts by the
one instar to the next. addition of segments basally.
374 POSTEMBRYONIC DEVELOPMENT
a) weight - terrestrial insect It is often true that different parts of the body grow at
different rates when compared with some standard such
1 2 3 4 5 adult
as total body length. If the rate of growth of the part, such
1000 0.25 as the head, is the same as that of the standard, growth is
relative growth
said to be isometric; if the rate is different from the stan-
(mg.mg-1.day-1)
weight (mg)
20 abdomen
growth rates are consistent over time, but this is not always
hind the case. The mesothorax of Dysdercus, increases at
femur
10 roughly the same rate as the body as a whole at the first
molt, but at later molts it exhibits positive allometry (Fig.
15.10b); the seventh abdominal segment increases at about
0
0 10 20 30 40 50 the same relative rate as the whole body in the early stages,
days but also exhibits marked positive allometry at the final molt
c) weight - aquatic insect as the genitalia develop. In none of the segments is growth
relative to the body as a whole uniform throughout larval
1 2 3 4 5 adult
life. Similar variations in relative growth rate occur in
150 Ectobius and are probably usual in larvae of hemimeta-
bolous insects.
weight (mg)
a) b)
instar
100
1 2 3 4 5
apical head
antennal length (%)
75 annuli
prothorax
meristal mesothorax
50 annuli
metathorax
pedicel
25 1
scape
2
0
abdominal
segments
larva 1 larva 2 larva 3 larva 4 adult 3
4
1.00 apical
length of region (mm)
annuli 5
0.75
scape
6
0.50 7
meristal
annuli marked positive allometry
slight positive allometry
slight negative allometry
0.20 marked negative allometry
1.5 2.0 2.5
length of antenna (mm)
Fig. 15.10. Allometric growth. (a) Changes in the relative proportions of different parts of the antenna of a hemimetabolous
insect in different stages of development. Above: representation of the whole antenna with lengths of different parts shown
as a percentage of the whole; below: changes in lengths of different parts plotted against the length of the whole antenna
(log/log scale) (Hemimerus, Dermaptera) (after Davies, 1966). (b) Diagram showing the growth rates of different parts of the
body relative to the growth of the body as a whole from one larval stage to the next in a hemimetabolous insect (Dysdercus,
Heteroptera) (after Blackith, Davies & Moy, 1963).
Regeneration Some insects are able to regenerate an 15.2.4.3 Growth of the tissues
appendage following its accidental loss. This occurs in The form of the cuticle is determined by the epidermis
Blattodea, some Orthoptera, Phasmatodea, some which may grow either by an increase in cell number or by
Hemiptera and larval holometabolous insects, but not in an increase in cell size. Cell numbers increase just before
Acridoidea. Regeneration of cuticular structures can only molting in many insects (see Fig. 16.15), but, in larval
occur at a molt as this is the only time at which new cuticle Cyclorrhapha, the increase in larval size during develop-
is produced. Consequently, it is restricted to larval stages; ment results entirely from an increase in the size of the epi-
regeneration of appendages does not occur in adults. If the dermal cells. In this case the nuclei also increase in volume
loss occurs early in a developmental stage, before the pro- as a consequence of endomitosis and this results in an
duction of molting hormone, the appendage reforms at the increase in the amount of DNA present in each nucleus.
next molt, but replacement of a limb lost after this does not Growth of the central nervous system of hemimeta-
occur until the following (next-but-one) molt. It grows at bolous insects does not involve the production of new
each successive molt, but generally remains smaller than a neurons except in the brain. In the terminal abdominal
normal appendage. ganglion of Acheta, for example, there are about 2100
Regeneration of muscles and parts of the nervous neurons at all stages of development. On the other hand,
system also occurs. the number of glial cells in the ganglion increases from
Review: Bullière & Bullière, 1985 – regeneration about 3400 in the first stage larva to 20 000 in the adult and
376 POSTEMBRYONIC DEVELOPMENT
a) contact chemoreceptors
80
60
number
40
20
0
L1 L2 L3 L4 adult
stage of development
Fig. 15.11. Average growth ratios from one larval stage to the
next for a range of hemimetabolous and holometabolous insects.
The growth ratio is the ratio of size in one stage to the size in the b) mechanoreceptors
previous stage averaged over all larval stages for each insect. The 300
data are derived primarily from measurements of head width
(after Cole, 1980).
200
the volume of the ganglion is increased 40-fold. In most number
holometabolous insects there is extensive reconstruction
100
of the nervous system at metamorphosis and
undifferentiated neuroblasts persist through the larval
period up to this time (see below). 0
Marked changes occur in the sensory system during L1 L2 L3 L4 L5 adult
larval development of hemimetabolous insects. Additional stage of development
mechanoreceptors and chemoreceptors are added to those Fig. 15.12. Changes in numbers of peripheral sensilla during the
already present at each molt (Fig. 15.12). The numbers of development of hemimetabolous insects. (a) Changes in the
ommatidia forming the compound eyes also increase. By numbers of contact chemoreceptors on the tip of the maxillary
contrast, the numbers of sensilla are constant through the palp of a grasshopper in successive stages of development
larval life of holometabolous insects and compound eyes (Bootettix, Orthoptera) (after Chapman & Fraser, 1989). (b)
are only present in adults (Chapman, 1982). Changes in the numbers of mechanosensitive filiform hairs on the
The musculature of most larval hemimetabolous prosternum of a locust in successive stages of development (after
Pflüger et al., 1994).
insects closely resembles that of adults and probably all the
adult muscles, including those that become flight muscles,
are represented at hatching. In addition, there may be tissues in this insect and in Drosophila have a constant
muscles that are operative only during molting and which number of cells and grow by cell enlargement. This
disappear after the final molt (section 10.2.4). The muscles enlargement is accompanied by endomitosis. In the
grow by an increase in fiber size between molts and by the midgut both processes occur; the epithelial cells enlarge,
addition of new fibers at molts (see Fig. 10.10). The mus- but ultimately break down during secretion and each is
culature of larval holometabolous insects is, by contrast, replaced by two or more cells derived from the regener-
usually fundamentally different from that of the adults. ative cells. In some insects the whole of the midgut epi-
During larval development, muscles increase in size, but thelium is replaced at intervals by regenerative cells
there is no basic change in their arrangement. (section 3.1.2). In general, it appears that tissues which are
As with the epidermis, an increase in the size of an destroyed at metamorphosis grow by cell enlargement
internal organ may result from an increase in cell size or in while those that persist in the adult grow by cell multi-
cell number, or sometimes both. The fat body of larval plication.
Aedes grows by an increase in cell number, but most other The development of the Malpighian tubules varies. In
LARVAL DEVELOPMENT 377
growth of internal organs, but some show cyclical activity adult are already attached to appropriate positions on the
which coincides with the molt. The fat body cells of larval cuticle. For instance, in adult Locusta, the promo-
Rhodnius, for example, exhibit a marked increase in RNA tor-extensor muscle of the mesothoracic wing is inserted
concentration and mitochondrial number just before a into the first basalar sclerite, but the equivalent muscle of
molt, and the ventral abdominal intersegmental muscles the metathoracic wing is inserted into both basalar scle-
become fully developed only at this time (section 10.2.4). rites. In the larva, although the sclerites are not devel-
In insects in which the Malpighian tubules increase in oped, the muscle in the mesothorax has one point of
number, mitosis and development of new tubules are attachment to the pleural cuticle, while that in the meta-
phased with respect to the molt. thorax has two.
Review: Caveney, 1985 In grasshoppers and dragonflies, all the flight muscles
are present in the larva, although some are lacking stria-
tions and are presumably nonfunctional. These muscles
15.3 METAMORPHOSIS
increase in size throughout the larval period and further
The changes that occur in the transformation of the larva changes occur in the young adult (section 10.2.2). Many
to the adult may be more or less extensive depending on muscles disappear after the final molt. They are necessary
the degree of difference between the larva and the adult. In for the process of molting (section 10.2.4) and their dis-
hemimetabolous insects, the changes are relatively slight; appearance is accompanied by the death of the motor
in holometabolous insects, the changes are very marked neurons supplying them. Other changes also occur in the
and a pupal stage is interpolated between the final larval nervous system. For example, changes in the arborization
stage and the adult. patterns of afferent sensory axons may occur within the
central nervous system even though the peripheral sensilla
15.3.1 Hemimetabolous insects remain functional (Pflüger et al., 1994). The effect of this
Epidermal mitosis and expansion only occurs at the time will be to alter the neural pathways of which the sensory
of a molt and, in hemimetabolous insects, progressive neurons form a part.
development of the wing buds occurs at each molt. Apart
from being small, the larval wing buds differ from the adult 15.3.2 Holometabolous insects
wings in being continuous sclerotizations with the terga The development of adult features in holometabolous
and pleura; the basal region of the wing is not membranous insects varies with the degree of modification of larval fea-
and no accessory sclerites are present. These appear at the tures involved. In Neuroptera and Coleoptera, where the
final molt. larvae have some resemblance to the adults, relatively little
In general, the wings arise in such a way that the lateral reconstruction occurs, but, in Diptera, the tissues are
margins of the wing buds become the costal margins of the almost completely rebuilt following histolysis and
adult wings (Fig. 15.3), but, in Odonata, the buds arise in phagocytosis of the larval tissues. This reconstruction
an erect position, the margin nearer the midline ultimately occurs in the pupa.
becoming the costal margin (Fig. 15.14a). The wing buds
of Acrididae originate as simple outgrowths of the terga, 15.3.2.1 Pupa
but at the antepenultimate molt they become twisted into All the features of the adult become recognizable in the
the position found in the Odonata. This twisting results pupa which consequently has a greater resemblance to the
from the lower epidermis growing more rapidly than the adult than to the larva. At the larva/pupa molt, the wings
upper. At the final molt the wings twist back so that the and other features that up to now have been developing
costal margins of the folded adult wings are ventro-lateral internally are everted and become visible externally
in position. although not fully expanded to the adult form (Fig. 15.5).
The genitalia develop progressively by modification of The appendages extend freely from the body in the pupae
the terminal abdominal segments, but with a more marked of some insects and this condition is known as exarate, but
alteration at the final molt (Fig. 15.14b). in other species the appendages are glued down by a secre-
Although accessory wing sclerites are not developed tion produced at the larva-pupa molt. This is the obtect
in the larva, the muscles that are attached to them in the condition and obtect pupae are usually more heavily scle-
METAMORPHOSIS 379
muscles
dorsal vessel trachea
b) external genitalia
INSTAR 1 INSTAR 2
sternum 8
ventral valve
sternum 9
dorsal valve
paraproct
cercus
0.5 mm 0.5 mm
sternum 8 sternum 7
ventral valve
sternum 8
sternum 9 (subgenital plate)
inner valve
dorsal valve cercus
rotized than exarate pupae. A further differentiation can Decticous pupae are always exarate. They occur in
be made on the presence or absence of articulated Megaloptera, Neuroptera, Trichoptera and some
mandibles in the pupa. When articulated mandibles are Lepidoptera. Some adecticous pupae are also exarate as in
present (the decticous condition), they have apodemes Cyclorrhapha, Siphonaptera and most Coleoptera and
fitting closely within the adult mandibular apodemes (Fig. Hymenoptera, but others are obtect. Most Lepidoptera,
15.15) and hence can be moved by the mandibular muscles Nematocera, Orthorrhapha, Staphylinidae, some
of the pharate adult. The alternative condition, with Chrysomelidae and many Chalcidoidea have obtect, adec-
immobile mandibles, is known as adecticous. ticous pupae.
380 POSTEMBRYONIC DEVELOPMENT
adult apodeme
adult apodeme
pupal apodeme pupal apodeme
adult cuticle
pupal cuticle adult mandible
exit tunnel
pupal mandible
obtect pupa
Protection of the pupa Most insect pupae are immobile passing along the abdomen from front to back. The larva
and hence vulnerable, and most insects pupate in a cell or subsequently enters an active wandering phase that ends
cocoon which affords them some protection. Many larval when it finds a suitable site in which to pupate. The first
Lepidoptera construct an underground cell in which to phase of cocoon formation is the construction of a scaffold
pupate, cementing particles of soil with a fluid secretion. of silk threads between leaves of the food plant and the
The larva of the puss moth, Cerura (Lepidoptera), con- production of a stalk which attaches the cocoon to the leaf
structs a chamber of wood fragments glued together to petiole. Subsequent behavior consists of a series of cycles
form a hard enclosing layer, and some beetle larvae pupate in which the insect weaves loops of silk using figure-of-
in cells in the wood in which they bore. Many larvae eight movements of the head to construct one end of the
produce silk which may be used to hold other structures, cocoon and then turns through 180 ° to form the other
such as leaves, together to form a chamber for the pupa, end. A complete layer of silk has been produced after a
but in some other species a cocoon is produced wholly period of about 14 h, and the insect turns from one end of
from silk (Fig. 15.16a). Silken cocoons are produced by the cocoon to the other at much shorter intervals (5 min
Bombycoidea amongst the Lepidoptera and by compared with 80 min at 23 °C) and at the same time coats
Siphonaptera, Trichoptera and some Hymenoptera. the inside of the cocoon with a liquid from the anus con-
Cocoon formation by the silkmoth, Antheraea, takes taining crystals of calcium oxalate. This liquid accumu-
about two days. It follows gut purging, in which the larva lates in the hindgut after purging and the calcium oxalate is
expels the gut contents by a series of waves of contraction produced by the Malpighian tubules.
METAMORPHOSIS 381
legs wing
antenna
wing
compound
abdomen eye
proboscis legs
cocoon
paddle
substratum
When the salivary glands produce silk, they also secrete where the pupae are suspended from a silk pad. These
compounds that will link the silk proteins in the same way exposed pupae exhibit homochromy (section 25.5.2.2)
that proteins are linked in the cuticle (section 16.5.3). whereas protected pupae are normally brown or very pale
These tanning agents, which are phenolic compounds in color.
derived from the food, are produced as glucosides and so
are inactive. The salivary gland also produces the enzymes Pupae of aquatic insects The behavior of aquatic insects
to activate the tanning agents, but, as the silk dries very on pupation varies considerably. Some larvae, such as
quickly, activation does not occur until it is rewetted by those of the aquatic Syrphidae and the beetle, Hydrophilus,
fluid from the caterpillar’s hindgut. At this time the chains leave the water and pupate on land, but many others, par-
of silk protein are linked together and the wall of the ticularly the aquatic Diptera, pupate in the water.
cocoon becomes stiff and colored yellow-brown. This Sometimes the pupae are fastened to the substratum. For
period of impregnation of the cocoon lasts for about an example, the pupae of Blepharoceridae have ventro-lateral
hour. Afterwards, more silk is added to the inside of the pads on the abdomen with which they attach themselves to
cocoon, but the spinning cycles are interrupted by periods stones, while Simuliidae construct open cocoons attached
of inactivity that become progressively longer until the to stones and rocks (Fig. 15.17a). The pupa projects from
larva becomes completely quiescent. the open end of the cocoon, which is constructed more
An exceptional protective structure is produced from strongly in faster flowing water than it is in a weak current.
the cuticle of the last stage larva by cyclorrhaphous Chironomidae pupate in the larval tubes or embedded in
Diptera. Procuticle is laid down throughout the last larval the mud, while Acentropus (Lepidoptera) forms a silken
stage at the end of which the larva shortens and the outer cocoon with two chambers separated by a diaphragm. The
part of the cuticle is tanned to form a rigid ovoid structure pupa lies in the lower chamber, which is air-filled.
known as the puparium (Fig. 15.16b). The process is called Other aquatic pupae obtain oxygen from the air, either
pupariation. Subsequently, after apolysis, the pupal/adult directly or indirectly. The pupae of most Culicidae and
head and appendages, previously concealed beneath the Ceratopogonidae are free-living and active. They are
larval epidermis, are everted and the pupal cuticle is buoyant so that, when undisturbed, they rise to the surface
secreted (Fristrom et al., 1991). The pupa remains inside and respire via prothoracic respiratory horns (Fig. 15.17b).
the puparium and the adult, when it emerges, escapes from If disturbed, movements of the anal paddles drive them
both the pupal and puparial cuticles. downwards. The pupae of some Culicidae and Ephydridae
A few insects form unprotected pupae. These are par- have their respiratory horns embedded in the tissues of
ticularly well known in the Nymphalidae and Pieridae, aquatic plants, obtaining their oxygen via the aerenchyma.
382 POSTEMBRYONIC DEVELOPMENT
epidermis
femur
differentiation tibia
center
larval coxa
cuticle
trochanter
c) 3 days d) late larva
femoro-tibial tarsus
bud coxa tibia
pupal
cuticle
trochanter
femur
tarsus
Fig. 15.18. Development of the adult leg of a lepidopteran at different times after the molt to the last larval stage and in the
pupa (Pieris) (based on Kim, 1959). (a)–(d) changes in the epidermis within the larval leg. The presumptive areas of the adult
leg are shown separated by dotted lines in d). (e) Fully developed leg (shaded) of the pharate adult within the pupal cuticle.
Significance of the pupa The occurrence of a pupa is pupa, the wings are everted and grow to some extent.
indicative of the broad differences which occur between Further growth occurs and the adult cuticle is laid down
larval and adult forms of holometabolous insects. It is a at the pupa–adult molt.
stage during which major internal reconstruction occurs The importance of the pupa in wing development and
and is of particular importance in permitting the develop- associated changes is emphasized by the absence of a pupal
ment and attachment of adult muscles to the cuticle and stage in the life histories of female Strepsiptera and
the full development of the wings. Coccidae, which are wingless and larviform. The males in
Most of the adult thoracic muscles are different from these groups are winged and have a pupal stage (see section
those of the larva. It has been suggested that muscles will 15.2).
only develop in an appropriate form and length if they Reviews: Hinton, 1948, 1963
have a mold in which to do so. The pupa provides a mold
for the adult muscles. Further, most muscles are attached 15.3.2.2 Development of adult features
to the cuticle by filamentous projections from the epicut- Epidermal structures If an adult appendage does not
icle (section 10.1.3) that can only develop at a molt, in this differ markedly from that of the larva it may be formed by
case the pupa to adult molt. a proliferation of the tissue within and at the base of the
Development of the wings internally within the larva larval organ. This occurs in the legs of Lepidoptera, for
is restricted by lack of space and this problem becomes example. Soon after the larva of the cabbage butterfly,
more acute as the insect approaches the adult condition Pieris, enters its final stage the epidermis of its thoracic
and the flight muscles also increase in size. Thus develop- legs becomes separated from the cuticle except at points of
ment can only be completed after the wings are everted muscle attachment. It is now free to thicken and fold. The
and, for this reason, two molts are necessary in the trans- first thickening, well supplied with tracheae, develops at
formation from larva to adult. At the first, from larva to the junction of the second and third leg joints (Fig. 15.18a)
METAMORPHOSIS 383
wing leg 3
disc disc haltere
disc
and from this differentiation center a wave of cell multi- enlarges the appendage forms and pushes into the cavity
plication spreads out (Fig. 15.18b,c). As a result of the (Fig. 15.20c) becoming folded as it increases in size. In
increase in area, the epidermis becomes folded and a par- Lepidoptera, the wings and antennae develop in peripodial
ticularly large fold develops basally. Later, when the epi- cavities, but, in Diptera, all the main ectodermal features
dermis expands to form the pupal leg, this basal fold of the adult develop in this way (Fig. 15.19c).
becomes divided by a longitudinal septum to form the At pupation, the appendage is everted and the peripo-
femur and tibia. Epidermis from the more proximal parts dial membrane comes to form part of the epidermis of the
of the larval leg forms the coxa and trochanter, and more general body wall (Fig. 15.20c,d). Evagination probably
distal tissue forms the tarsus. Further differentiation con- results from a rearrangement of the cells of the disc which,
tinues in the pupa to produce the adult leg (Fig. 15.18e). at the same time, also tend to increase in surface area. This
Where the difference between larval and adult organs is process is initiated by an increase in 20-hydroxyecdysone
more marked the adult tissues develop from epidermal in the hemolymph; at earlier molts, when the titer of this
thickenings called imaginal buds or discs. The founder hormone also increases, evagination is probably inhibited
cells comprising these discs divide to form clones. Since by juvenile hormone. At some stage, the discs acquire the
the production of adult organs is restricted to small groups ‘competence’ to undergo metamorphosis. Prior to this,
of cells the remainder of the epidermis is free to undergo metamorphosis does not occur even in the appropriate
larval modifications. The discs may be regarded as islands humoral environment. The acquisition of competence
of embryonic tissue which remain undifferentiated until appears to be associated with the number of divisions that
they give rise to the adult structures. They do not produce the cells of the disc have undergone.
cuticle in the larva and the cells continue to divide between The details of development of the imaginal discs vary
molts (Fig. 15.19a), not just at the time of the molt as from one insect to another and from organ to organ.
occurs with larval epidermal cells. Where an appendage is present in the larva as well as the
The imaginal disc commonly becomes invaginated adult the imaginal disc is closely associated with the larval
beneath the larval epidermis forming a cavity known as the structure. Thus, in Pieris, the adult antenna is first appar-
peripodial cavity (Fig. 15.20b). It is lined with epidermis ent in the first stage larva as a thickening of the epidermis
(the peripodial membrane) and as the imaginal disc at the base of the larval antenna. The cells divide and, in
384 POSTEMBRYONIC DEVELOPMENT
Fig. 15.20. Development of an adult leg in Drosophila. (a) Fate map of a leg disc (after Schubiger, 1971). (b)–(d) Sections
through the disc at different times after pupariation showing the elongation and eversion of the leg (from Fristrom &
Fristrom, 1993).
the succeeding stages, an invagination is produced which Pieris, the wing imaginal discs are apparent in the
pushes upwards, deep into the larval head. In the fifth embryo and invaginate in the second and third larval
stage larva, the adult antennal tissue grows more quickly stages. During the fourth stage, the wing starts to
than the peripodial membrane, so that it is thrown into develop in the peripodial cavity, finally becoming exter-
folds, and towards the end of the larval stage the larval nal at the larva–pupa molt. In Drosophila, on the other
antenna starts to degenerate and is invaded by imaginal hand, invagination of the peripodial cavity is complete
cells. When the peripodial cavity (which opens by a slit on before the larva hatches, but the wing itself does not
the front of the epidermis of the head) evaginates, the develop until the second larval stage, growing more
antenna is carried to the outside and the peripodial mem- extensively in the third stage.
brane now forms a part of the wall of the head. The maxilla During development, the cells of each imaginal disc
develops in an essentially similar way, but very little become programmed for their ultimate phenotypic
development of the labium takes place until the fifth larval expression in the adult. They are said to become deter-
stage. mined, and their subsequent development is fixed; they
The wings also develop from imaginal discs (Fig. will produce the same structure even if they are moved
15.21). In some Coleoptera, they form as simple evagina- experimentally to another position on the appendage.
tions of the epidermis beneath the larval cuticle, but More detailed features are not determined until after the
more usually they develop in peripodial cavities. In more basic characters. For example, the dorsal and ventral
METAMORPHOSIS 385
Fig. 15.21. Development of a forewing in Drosophila. (a) Fate map of a wing disc (after Bryant, 1975). (b) Section through the
disc at the time of pupariation (from Fristrom & Fristrom, 1993). (c) Section through the disc two hours after pupariation
(from Fristrom & Fristrom, 1993).
surfaces of the wing are determined before the details of the pupal cuticle is laid down. After this the upper and
the pattern, and cells become committed to a segment of a lower surfaces of the wing are forced apart by an increase
leg before a specific structure on that segment. Some in blood pressure (Fig. 15.22c,d). The cells at first become
degree of determination of the adult tissues may already stretched across the gap as narrow threads connecting the
be apparent in the embryo, and determination of wing two surfaces, but these connections are finally broken
regions is advanced at the time of pupariation (Fig. 15.21). except at the wing margins. A less extensive inflation
In Drosophila, cells along the dorso-ventral boundary of occurs in Tenebrio (Coleoptera) and Habrobracon
the wing have a critical organizational role (Kim, Irvine & (Hymenoptera). Perhaps the inflation has the effect of
Carroll, 1995). expanding the newly formed pupal cuticle to the greatest
The internal development of the wings is complex, possible extent so that the development of the adult wing
involving great expansion and the formation of the veins. can proceed.
The development of a Drosophila wing is used here as an Following inflation, the wing flattens again. The epi-
example. When the wing evaginates at pupation, the upper dermal layers on the two sides first become apposed round
and lower surfaces have already come together although the edges (Fig. 15.22e) and then the contraction spreads
they remain separated along certain lines called lacunae inward so that a flat double sheet of cells is produced (Fig.
(Fig. 15.22a,b). Four lacunae run the length of the wing 15.22f). During this process the definitive wing veins are
rudiment, the second dividing into two distally. A nerve formed along lines where the two epidermal layers remain
and a trachea enter the second lacuna, and at about this separated (Fig. 15.22g). The veins are at first wide chan-
stage, some six hours after the formation of the puparium, nels, but they become narrower as the wing continues to
386 POSTEMBRYONIC DEVELOPMENT
a) e)
lacuna veins
forming
f)
b) lacuna
basal ends
c) of cells g) definitive
veins
epidermis
pupal
cuticle pupal
d) h) cuticle
basal processes
becoming broken adult cuticle veins
Fig. 15.22. Diagrammatic transverse sections of a developing forewing of Drosophila (after Waddington, 1941): (a),(b)
successive stages in the larva before pupation; (c)–(g) successive stages in the pupa; (h) pharate adult.
expand. Cell division proceeds actively, especially above the larval epidermis is replaced varies. In Coleoptera there
the veins, so that here the cells become crowded and is no extensive replacement, but in Hymenoptera and
columnar, while elsewhere they are flattened. The fully Diptera the epidermis is completely renewed from imagi-
developed wing finally secretes the adult cuticle (Fig. nal cells. The epidermis of the head and thorax are formed
15.22h). by growth from the imaginal appendage discs, while the
Even in the imaginal discs, some programmed cell abdominal epithelium is formed from special groups of
death (apoptosis) occurs in the course of differentiation. cells called histoblasts. In Drosophila, the abdominal seg-
This is especially obvious where normal adult structures ments have pairs of dorsal, ventral and spiracular histo-
are of reduced size. The female vaporer moth, Orgyia, for blasts (Fig. 15.19c). These initially comprise 5–15 cells
example, has only vestigial wings, but up to the pupal molt which remain unchanged throughout larval development,
her wings develop normally as imaginal discs. Then, but after pupariation the cells start to divide. They gradu-
during apolysis, as the epidermis retracts from the pupal ally replace the larval cells, but at no time is there any dis-
cuticle, extensive cell death occurs so that the wings continuity in the epidermis. The larval cells are completely
become greatly reduced in size. Cell death on a much replaced and are sloughed off into the body cavity and
smaller scale occurs in the developing wings of the male phagocytosed.
which is fully winged (Nardi, Godfrey & Bergstrom, Reviews: Campbell & Tomlinson, 1995 – axial determination in
1991). legs; Cohen, 1993 – Drosophila imaginal discs; Fristrom &
When the imaginal appendages are everted from the Fristrom, 1993 – Drosophila epidermis; Fristrom et al., 1991 –
peripodial cavities at the time of pupation, the peripodial pupal cuticle in Drosophila; Larsen-Rapport, 1986 –
membrane contributes to the general epidermis of the determination; Oberlander, 1985 – imaginal discs; Williams &
adult body wall (Figs. 15.20, 15.21). The extent to which Carroll, 1993 – determination
METAMORPHOSIS 387
Muscles The muscular system usually undergoes exten- the dilator muscles of the pharynx remain unchanged until
sive modification at metamorphosis and the muscles fall after pupation. They are apparently important in the
into four categories: evagination of the head region of the insect at pupation,
and only degenerate after this has occurred. In addition,
1 Larval muscles may pass unchanged into the adult one pair of muscles persists in each abdominal segment for
2 Existing larval muscles are reconstructed about half the pupal period. They may help to establish the
3 Larval muscles may be destroyed and not replaced segmentation of the pupal abdomen by telescoping each
segment into the preceding one.
4 New muscles, not represented in the larva, may be
The first sign of muscle degeneration is liquefaction of
formed.
the peripheral parts of the fiber. This is followed by
The adult muscles of some flies are already present in separation of the fibrils and, in the flour moth, Ephestia,
the larva as rudimentary non-functional fibers. The dorsal phagocytes penetrate the sarcolemma and assist the
longitudinal muscles in Simulium, for instance, are only destruction. The sarcolemma breaks down and the
about four microns in diameter in the first stage larva. They muscles separate from their attachments and fragment, the
grow throughout the larval period and their nuclei increase remains being consumed by phagocytes.
in number. During the pharate pupal period the muscle New muscles are always formed by free myoblasts that
rudiment becomes divided to produce the definitive aggregate to form multicellular groups within which cells
number of fibers and myofibrils appear for the first time. fuse to form the multinucleate muscle fibers. Where the
They continue to grow until some time after the final molt. new muscle is associated with an existing motor neuron
Reconstruction of larval muscles occurs in two ways. In that becomes respecified (see below), the myoblasts may
the Neuroptera, Coleoptera and some Lepidoptera, larval migrate along the axon to their definitive positions and the
muscles contain two sets of nuclei, the functional larval neuron may influence the rate of myoblast proliferation
nuclei and other, small, nuclei which are scattered through (Currie & Bate, 1991; Fernandes, Bate & Vijayraghavan,
the cytoplasm. At metamorphosis the small nuclei multiply 1991). Many of the muscles that are produced during the
and, with associated cytoplasm, form myocytes. These pupal period have only short lives in Diptera and
migrate into the body of the muscle and associate in strands Lepidoptera. These are the muscles specifically associated
to form new fibers. In Diptera, and some Lepidoptera and with eclosion which break down after the adult insect has
Hymenoptera, on the other hand, myoblasts originating emerged from the pupal cuticle (see Fig. 10.14).
outside the larval muscle are concerned in the production Reviews: Fernandes & Keshishian, 1995; Schwartz, 1992 –
of adult muscle, adhering to the outside or penetrating the programmed cell death
sarcolemma in order to form new fibers. The dorsal longi-
tudinal flight muscles of adult Drosophila are formed by Nervous system The central nervous system of
new myoblasts, but larval muscles form a scaffold that holometabolous insects is extensively restructured at
determines the appropriate development of the adult metamorphosis. The brain becomes considerably
muscles (Farrell, Fernandes & Keshishian, 1996). enlarged, mainly due to the development of the antennal
Most larval muscles are completely histolyzed and dis- and optic lobes in relation to the much larger antennae of
appear during the early pupal period, but the precise adult insects and the appearance of compound eyes. In
timing varies because some larval muscles have specific most holometabolous insects, particularly those that are
functions in pupal development or adult eclosion and are more specialized, fusion of some ventral ganglia com-
destroyed much later than others. For example, the larval monly occurs at metamorphosis. This condensation is
leg muscles of Manduca start to degenerate when the larva effected by a forward movement of the more posterior
enters its wandering phase and degeneration is complete by ganglia resulting from the shortening of the inter-
the time the larva pupates (Consoulas, Anezaki & Levine, ganglionic connectives. For instance, the larva of Manduca
1997). Some abdominal muscles, however, do not degener- has, in addition to the head ganglia, three thoracic and
ate until after pupation. In Drosophila, most muscles of the seven separate abdominal ganglia. In the adult, the meso-
head and thorax start to break down before puparium and meta-thoracic ganglia are fused with the first two
formation and are fragmented before the larva pupates, but abdominal ganglia to form a compound ganglion close
388 POSTEMBRYONIC DEVELOPMENT
behind the prothoracic ganglion. The next three abdomi- The sensory system is almost entirely renewed at meta-
nal ganglia remain separate, but the last three fuse morphosis in holometabolous insects. The compound eyes
together to form another compound ganglion (Fig. and antennae of the adult are completely new structures,
15.23a). In the course of these changes the perineurium is and this is true of the sensilla associated with the mouth-
histolyzed and the neural lamella digested, the former parts, at least in a majority of insects. It is known, however,
being redeveloped from remaining glial cells. The higher that a few mechanoreceptors persist during the pupal stage
Diptera are exceptional in having a more condensed of Manduca and some stretch receptors and chordotonal
central nervous system in the larva than in the adult. organs are still present in the adult.
Over 90% of the neurons in the nerve cord of adult Reviews: Levine, Morton & Restifo, 1995 – molecular biology;
Drosophila develop during the larval period from groups of Truman, Thorn & Robinow, 1992 – programmed cell death;
neuroblasts that persist from the embryo. In the first stage Weeks & Levine, 1992 – control
larva of Drosophila, there are 47 neuroblasts in each tho-
racic neuromere, but only six in each abdominal neuro- Alimentary canal The alimentary canal is extensively
mere. Manduca has over 20 neuroblasts in each of the remodelled at metamorphosis in species that have different
thoracic ganglia, but only four in the abdominal neuro- larval and adult diets. In larval Lepidoptera, for example,
meres behind the first. These cells start to divide at the gut is relatively simple and the midgut occupies most
different times during larval development. The most rapid of the body cavity, but the adult has a large crop and rectal
division occurs in the final larval stages (Fig. 15.23c). Some sac and only a small midgut (Fig. 15.24a,b). This change is
of these cells die just before and during pupal development, associated with the change from leaf-feeding, with
but, despite this, the neuroblasts contribute over 2500 new continuous access to food, to fluid-feeding, with the need
interneurons to each of the thoracic ganglia and about 50 to to store nectar in the crop between feeds and the require-
each abdominal ganglion in Manduca. Similar numbers are ment to digest and absorb only sugars. Reconstruction of
produced in Drosophila. All these new cells become inter- the stomodeum and proctodeum results from the renewed
neurons; probably no new motor neurons are formed activity of the larval cells without any accompanying cell
(Booker & Truman, 1987; Truman & Bate, 1988). destruction in Coleoptera, but, in Lepidoptera and
The motor neurons already present in the larval gan- Diptera, new structures develop, at least partly, from pro-
glion have two possible fates, depending on the muscles liferating centers known as imaginal rings at the inner ends
which they innervate: of the foregut and hindgut. The larval cells are sloughed
into the body cavity.
1 If the larval muscle degenerates, but a new muscle
The midgut is probably completely renewed in all
develops in a similar position, the neuron may persist
holometabolous insects, usually being reformed from the
and innervate the new muscle. It is said to be
regenerative cells at the base of the epithelium. These cells
respecified.
proliferate and form a layer round the outside of the larval
2 If the larval muscle is destroyed and not replaced, the
cells which thus come to lie in the lumen of the new ali-
motor neuron dies. This may occur at various times
mentary canal. Sometimes this process occurs twice, once
during metamorphosis. About 16% of all the motor
on the formation of the pupa and again when the adult
neurons in the abdominal ganglia of Manduca die soon
tissues are forming. It is suggested that the special pupal
after pupation following the deaths of their target
midgut enables the insect to digest the sloughed remains of
muscles.
the larval midgut so that these can be assimilated and used
Respecification of neurons occurs in relation to leg and in the reconstruction. In Manduca, the newly formed epi-
flight muscles as well as to the newly formed abdominal thelium contains large vacuoles containing the enzyme,
intersegmental muscles. For example, the neuron inner- lysozyme, which is discharged into the lumen when the
vating a femoral flexor muscle in the larva of Manduca is epithelium is complete (Fig. 15.24c). It is presumed to
respecified to innervate the femoral extensor muscle in the have an antibacterial function (Russell & Dunn, 1991).
adult leg. This involves regression and then regrowth of
the dendritic arborization in the ganglion and the remak- Malpighian tubules Sometimes the larval Malpighian
ing of contact with the new target muscle by the axon. tubules remain unchanged in the adult, or slight
METAMORPHOSIS 389
a) central nervous
system b) dendritic arborization
LARVA ADULT 1 larva 5 pupa
brain
extent of arbor
subesophageal
thoracic 1
0.5
thoracic 2
thoracic 3
abdominal 1 0
5 10 15 20 25 30
abdominal 2 days
60 larva
3 larva 4 larva 5 pupa adult
abdominal 4
number of cells
40
abdominal 5
20
abdominal 6 0
0 5 10 15 20
days
abdominal 7 + 8
Fig. 15.23. Metamorphosis of the central nervous system of Manduca. (a) Brain and ventral nerve cord of the larva and adult
showing the fusion of ganglia. (b) Changes in the form of an abdominal motor neuron from larva to adult. The extent of the
arbor is expressed on an arbitrary scale (from Truman & Reiss, 1988). (c) Changes in the number of neurons produced from a
neuroblast nest in an abdominal ganglion. The decline in cell number at pupation is due to the deaths of many cells (after
Booker & Truman, 1987).
modifications may occur as in the Lepidoptera. larva–pupa molt through the activity of hemocytes.
Caterpillars have a cryptonephridial arrangement of the Subsequently, in Drosophila, the cells persist independently
Malpighian tubules (Fig. 18.14), but at metamorphosis the but are progressively histolyzed. Some may persist in the
parts associated with the rectum are histolyzed while the adult’s head, but the bulk of the adult fat body is formed
more proximal parts form the adult tubules. In Coleoptera, from mesenchyme cells on the inside of the imaginal discs.
the tubules are rebuilt from special cells in the larval In Lepidoptera, the cells of the peripheral fat body which
tubules, while, in Hymenoptera, the larval tubules break synthesize storage proteins in the caterpillar are destroyed,
down completely and are replaced by new ones developing but those of the perivisceral fat body that accumulate the
from the tip of the proctodeum. proteins reassociate to form the adult fat body.
Review: Haunerland & Shirk, 1995
Fat body The fate of the fat body at metamorphosis has
been most fully studied in Lepidoptera and Diptera. In both Other systems In general, the tracheal system shows little
groups, the cells of the fat body become disassociated at the change other than the development of new branches to
390 POSTEMBRYONIC DEVELOPMENT
a) larva a) b)
crop midgut rectum ANTERIOR ANTERIOR
spiracle
tuft of
tracheae tracheoles
coils of extending
esophagus Malpighian ileum tracheoles
tubule
dorsal longitudinal
muscle
main tracheal
rectal trunk
b) adult sac
extended epidermal
crop cells
POSTERIOR POSTERIOR
coiled d)
esophagus tracheoles
ileum c)
midgut tracheoles
uncoiling
Malpighian
tubule
trachea
c) lysozyme
start of ecdysis to
wandering pupa
in gut lumen Fig. 15.25. Metamorphosis of the tracheal system in the thorax of
100
Calliphora (after Houlihan & Newton, 1979). (a),(b) Diagrams of
enzyme activity
the right half of the thorax of the pharate adult three and four
days after pupariation showing the tracheal supply to the
50 in epithelium developing dorsal longitudinal muscle. At first, the muscle is very
short, and connects with long extensions of the epidermal cells.
As it elongates, the extensions become shorter. (c),(d) A tuft of
tracheoles arising from the end of a trachea. The tracheoles are
0
coiled on day 3 (c), but have uncoiled by day 4 (d).
6 8 10 12
time after ecdysis to instar 5 (days)
coiled about a third of the way through the puparial period
Fig. 15.24. Metamorphosis of the alimentary canal in a (Fig. 15.25). Up to this time the developing adult flight
lepidopteran: (a) larval gut; (b) adult gut; (c) lysozyme activity in muscles are still very short and their development is not
the midgut epithelium and lumen during the final larval and early
dependent on an oxygen supply. Subsequently, however,
pupal stages of Manduca (after Russell & Dunn, 1991).
they elongate rapidly and the tracheoles uncoil, extending
with the muscle fibers whose metabolic processes at this
accommodate the particular needs of the adult, such as the time are at least partially dependent on aerobic respiratory
supply to the flight muscles, and the elimination of some processes. Subsequently, the adult tracheal supply devel-
specifically larval elements. In cyclorrhaphous Diptera, ops from tracheoblasts largely independently of the pupal
however, an extensive reconstruction occurs. The pupal supply, but it remains fluid-filled until about three hours
tracheal system consists of four main tracheal trunks before eclosion. The filling of the adult tracheae with air
which extend into the head and as far as the anterior seg- corresponds with a sharp increase in oxygen consump-
ments of the abdomen from the thoracic spiracle. From tion, partly associated with increased metabolic activity in
these main trunks, tufts of fine, unbranched tracheae arise the tissues and partly with an increase in movements by
and each ends in several tracheoles which become tightly the fly.
METAMORPHOSIS 391
20
15.3.3 Eclosion
The escape of the adult insect from the cuticle of the pupa
or, in hemimetabolous insects, of the last larval stage is
10
known as eclosion. Where the pupa is enclosed in a cell or
cocoon the adult also has to escape from this.
cocoon
cutter
permanent
mandible
muscle cuticle of
head
oral secretion containing potassium hydroxide which escape from the puparium (Fig. 15.27a). It can be expanded
softens one end of its cell of agglutinated wood chips. This in the newly emerged fly by blood forced into the head from
enables the adult insect to push its way out protected by the the thorax and abdomen and is then withdrawn again by
remnants of the pupal cuticle. The silkmoths Bombyx and muscles which force blood back to the thorax. Pressure of
Antheraea produce a proteinase which softens the silk wall the ptilinum splits off the cap of the puparium and, if the
of the cocoon sufficiently for the adult to push its way out. puparium is buried in the soil, the ptilinum is also used by
In Antheraea, the proteinase is secreted on to the surface of the fly to dig its way to the surface. Once the fly’s cuticle has
the galeae two days before eclosion. It dries, forming a semi- hardened, the ptilinum is no longer eversible and the
crystalline encrustation. At the time of eclosion a liquid is muscles associated with it degenerate. Its position is indi-
secreted from labial glands which open by a single median cated in the mature fly by the ptilinal suture.
pore just below the mouth. This liquid dissolves the enzyme The degree of hardening that these insects undergo
and wets the inside of the cocoon. It contains potassium and before escaping from the cocoon varies. In some, most of
functions as a buffer keeping the enzyme solution at about the cuticle remains soft until after eclosion, but some parts,
pH 8.5. The enzyme digests the sericin coating of the silk so particularly those involved in locomotion, harden before-
that the fibroin threads are readily separated. A few hand. Thus, in Calliphora, the legs and apodemes harden,
Noctuidae also produce softening secretions. so do the bristles which protect the soft cuticle, and such
Cyclorrhaphous Diptera have an eversible sac called the specialized parts as the halteres, antennae and genitalia.
ptilinum at the front of the head which assists in their The remainder of the cuticle does not harden until after it
METAMORPHOSIS 393
is expanded when the insect is free. In Lepidoptera, pupae then escape from their cocoons or larval tubes and
however, the body does not expand greatly after eclosion rise to the surface. Many Trichoptera swim to the surface
and hardening of the cuticle is extensive before the insect as pharate adults, the middle legs of the pupae of these
emerges from the cocoon, although the wings remain limp. species being fringed to facilitate swimming, and the insect
Other insects emerge from the pupa and harden fully may continue to swim at the surface until it finds a suitable
before making their escape from the cocoon and they may object to crawl out on. In other Trichoptera, the pharate
have specialized features to assist this. Coleoptera and adults crawl up to the surface while the last stage larvae of
Hymenoptera use their mandibles to bite their way out. Odonata and Plecoptera crawl out onto emergent vegeta-
Some weevils of the subfamily Otiorrhynchinae have an tion so that the adult emerges above the water. Larval
appendage, known as the false mandible, on the outside of Ephemeroptera also come to the surface, but the form that
the mandible (Fig. 15.27b), which is used in escaping from emerges is a subimago, not the imago. The subimago
the cocoon and then, in most species, falls off. Amongst resembles the imago, but its legs and caudal filaments are
the Cynipidae (Hymenoptera), which do not feed as shorter and the wings are translucent instead of transpar-
adults, the sole function of the adult mandibles is to allow ent and are fringed with hairs. The subimago flies off as
the insect to escape from the host in which the larva soon as it emerges, but settles a short distance away and
pupated. soon molts to the imago. This is the only known example of
The cuticle of fleas also hardens before they escape a fully winged insect undergoing a molt.
from their cocoons and they may remain in the cocoon for The act of eclosion at the surface, in mosquitoes,
some time after emergence. Their escape is stimulated by results from the pharate adult swallowing air. Before the
mechanical disturbances and in many species is facilitated pupal cuticle is split, the air is probably drawn from the
by a cocoon cutter on the frons. In Trichopsylla, the cocoon space between the adult and pupal cuticles and is derived
cutter is deciduous (Fig. 15.27c). Finally, in the males of from air drawn into the tracheal system through the respi-
Strepsiptera, the mandibles are used to cut through the ratory horns of the pupa. A comparable process probably
cephalothorax of the last stage larva in which pupation occurs in other insects with aquatic pupae.
occurs. The larval cephalothorax is earlier extruded
through the cuticle of the host so that the adult insect can 15.3.3.3 Timing of eclosion
easily escape (Hinton, 1946). It is important that eclosion is timed so that an insect’s life
history is synchronized with suitable environmental
15.3.3.2 Eclosion of aquatic insects conditions and so that the meeting of the two sexes is facil-
Of the insects that pupate under water, some emerge itated. Synchrony with the environment results from the
under water and swim to the surface as adults; in others, common reaction to the environment of the members of
the pupa rises to the surface before the adult emerges. In the species. Temperature is particularly important since,
the Blepharoceridae, the adult undergoes some degree of to a large extent, it governs the rate of development and the
hardening within the pupal cuticle, so that as soon as it activity of the insect. In long-lived species, a diapause may
emerges it rises to the surface and is able to fly. Simulium also be important in synchronizing eclosion so that the
and Acentropus also emerge beneath the surface, but come sexes meet (see below).
up in a bubble of air. In Acentropus, this is derived from the Apart from these general seasonal effects, many insects
air in the cocoon, while Simulium pumps air out into the emerge at particular times of day, often at night or in the
gap between the pupal and adult cuticles. Thus the adult early morning. This probably gives the insect some degree
emerges into a bubble of air and is able to expand its wings of protection against predators while it is at its most
before rising to the surface. vulnerable in the period before it is able to fly. Thus, in
The pupae of Culicidae are buoyant, while some other Britain, the last stage larvae of Anax (Odonata) which are
insects, such as Chironomus, whose pupae are normally ready to molt leave the water between 20.00 and 21.00
submerged, increase their buoyancy just before emergence hours and by 23.00 hours most adults have emerged and
by forcing gas out of the spiracles into the space beneath are expanding their wings. The timing of emergence of
the pupal cuticle, or by increasing the volume of the tra- Sympetrum (Odonata) and most tropical dragonflies is
cheal system. Aided by backwardly directed spines, these similar, although some temperate species emerge during
394 POSTEMBRYONIC DEVELOPMENT
the day, perhaps because activity is limited by low temper- This probably reflects, in part, the smaller size of many
ature at night. male insects.
Moths are also known to emerge at particular times of
day, the timing being controlled by the eclosion hormone
15.4 CONTROL OF POSTEMBRYONIC
acting in response to photoperiod or temperature cycles
DEVELOPMENT
and differing in its time of release from species to species.
For example, with a cycle of 17 h light:7 h dark, Hyalophora Cuticular growth and changes in form only occur when an
escapes from the pupal cuticle in the first hours of the light insect molts. These processes are governed, primarily, by
period, while Antheraea pernyi does so towards the end of two classes of hormone: juvenile hormone and molting
the light period. The emergence of Manduca is also affected hormones (ecdysteroids) (Chapter 21). Molting is induced
by light, but is regulated more effectively by an increase in and regulated by ecdysteroids. As their titer in the hemo-
temperature of 3 °C or more. This is to be expected since lymph rises, the epidermal cells exhibit a complex pattern
the insect pupates beneath the soil surface. of DNA and RNA synthesis. This is known as the pre-
It is probable that the time of emergence of many paratory phase; it ends with division of the epidermal cells
insects is determined by entrainment to light or tempera- (Fig. 15.28 shows some of the processes involved at the molt
ture cycles. This is true of the moths described above and to adult in Manduca; similar changes occur in the epidermis
of Drosophila. In other cases, emergence may be a direct and cuticle at all molts). Except for cells in the imaginal
response to environmental conditions, even if these act at discs of holometabolous insects, this is the only time when
some previous time. For example, synchrony within a mitosis occurs in epidermal cells. At this time, with the
brood of Aedes taeniorhynchus is brought about by a ten- ecdysteroid titer approaching its peak, apolysis occurs and
dency for the larvae to pupate at about sunset, but different the epidermal cells produce the new epicuticle. Then, the
broods emerge at different times depending on the tem- falling titer of ecdysteroid leads to the production of chitin
perature during the pupal period (Clements, 1992). and the proteins of the new procuticle. Ecdysis follows soon
It is common for male insects to emerge as adults a little afterwards. (For a more complete account of the cuticular
before the females, although the difference is not great. changes occurring during a molt, see section 16.4.)
CONTROL OF POSTEMBRYONIC DEVELOPMENT 395
prothoracicotropic hormone
ecdysteroids
commitment
peak
critical periods
juvenile hormone
1 2 3 4 1 2 3 4 5 6 7 8 9 10 1 2 3 4 5 6 18 19 1
time in each stage (days)
Fig. 15.30. Changes in hormone titers regulating molting and metamorphosis in a holometabolous insect. At the molt from
larva to larva, juvenile hormone is present during the critical period; at the molt from larva to pupa, no juvenile hormone is
present at the first critical period. The second critical period of sensitivity to juvenile hormone in the fifth stage larva
regulates development of the imaginal discs. Eclosion hormone and bursicon are produced for a brief period before and
after each ecdysis (based on data for Manduca, Lepidoptera).
the larva is committed to molting to another larva. If head the presumed neural signal produced by size. Each period
width exceeds 5 mm, however, the larva is committed to of ecdysteroid production is preceded by a peak of PTTH.
become a pupa at the next molt (Fig. 15.32). Head size may In the final stage larva of Manduca, and perhaps also of
not be the relevant parameter for the insect, but it seems other insects, the release of PTTH is inhibited by a high
likely that some aspect of size is relevant. It is not known titer of juvenile hormone in the hemolymph although in
how the insect is able to assess its size, or how the informa- earlier larval stages PTTH is released in the presence of
tion is transmitted within the body. If the larva of Manduca juvenile hormone.
is committed to pupate, juvenile hormone production is In Manduca, PTTH release only occurs within a
switched off when the insect reaches a weight of about 5 g. certain period of the day, extending from just before until
sometime after lights-out in the laboratory. Its production
15.4.2 Production of ecdysteroid hormones is said to be gated (Fig. 15.33). This probably ensures that,
The prothoracic gland is stimulated to produce ecdysone under natural conditions, the insect molts during the
by the prothoracicotropic hormone (PTTH) (Chapter 21). night. Photoperiodic gating of PTTH secretion is proba-
Release of this hormone, usually via the corpora cardiaca bly a common phenomenon.
(but from the corpora allata in Lepidoptera), results from Ecdysteroid hormones regulate many other activities
CONTROL OF POSTEMBRYONIC DEVELOPMENT 397
EPIDERMIS CUTICLE
BRAIN
PROTHORACIC
GLAND
20-hydroxyecdysone
6 PTTH
EH ETH PTTH
ecdysone
5 1 2 3 4
CORPUS
CARDIACUM
EPITRACHEAL
GLANDS 7
EH
ETH
9 7a
5a EH
bursicon
BODY WALL
MUSCLES
HEART
pre-eclosion
behavior
CCAP
CCAP CCAP
8 8a
VENTRAL
eclosion GANGLION
behavior
HEMOLYMPH
neurosecretory cell
interneuron
motor neuron
CONTROL OF ECDYSIS
5 ecdysis triggering hormone causes release of eclosion hormone
5a ecdysis triggering hormone switches on pre-eclosion behavior
6 positive feedback loop between ETH and EH results in massive release of EH
7 central release of EH causes release of CCAP
7a EH acting via hemolymph plasticizes cuticle
8 CCAP switches on eclosion behavior and switches off pre-eclosion behavior
Fig. 15.31. The hormones involved in regulation of events at a molt. Juvenile hormone is not shown. Names of hormones are
italicized. CCAP, crustacean cardioactive peptide; EH, eclosion hormone; ETH, ecdysis triggering hormone; PTTH,
prothoracicotropic hormone.
398 POSTEMBRYONIC DEVELOPMENT
pupation 8
larva continues to feed
8 and grow until
wandering begins
6
a) pre-eclosion b) eclosion
segment
left
4
right
left
5
right
left
6
right
10 s
Fig. 15.34. Patterns of motor activity in nerves to the abdominal muscles initiated by hormones at eclosion of an adult moth
(Manduca) (see Fig. 15.31) (based on Truman, 1978). (a) Pre-eclosion behavior is switched on by ecdysis triggering hormone.
(b) Eclosion behavior is switched on by crustacean cardioactive peptide, the release of which is stimulated by eclosion
hormone.
Eclosion hormone is released locally within the central 15.34b). After eclosion, this behavior is inhibited by higher
nervous system as well as into the hemolymph, and this centers in the central nervous system.
leads to the release of CCAP in the ventral ganglia. Eclosion hormone also regulates plasticization of the
Crustacean cardioactive peptide switches off pre-eclosion cuticle of the wings, the release of bursicon, and break-
behavior and switches on eclosion behavior. Acting via the down of the eclosion muscles in silkmoths.
hemolymph, it also causes an accelerated heartbeat. Reviews: Hesterlee & Morton, 1996; Horodyski, 1996; Truman,
The programs of motor neuron activity which produce 1985, 1988; also see Ewer, Gammie & Truman, 1997
pre-eclosion and eclosion behavior are built into the
abdominal ganglia and, in some insects, can be produced 15.4.4 Controlling expansion and sclerotization
even in the isolated abdominal nerve cord. Pre-eclosion After ecdysis, wing spreading behavior is triggered via the
behavior consists of a series of abdominal rotations. These subesophageal ganglion. Tonic contraction of the
are produced by the muscles of the two sides contracting in abdomen forces blood into the wings and wing spreading
antiphase, while those of successive segments contract begins. The start of this activity triggers the release of the
together (Fig. 15.34a). This behavior, which probably hormone bursicon from the neurohemal organs associated
serves to free the adult abdomen from the overlying pupal with the abdominal ganglia. Bursicon first produces a
cuticle, lasts about 30 minutes in Hyalophora. It is followed further increase in the plasticity of the wing cuticle and
by a period of quiescence of about the same duration and then initiates tanning. The release of bursicon is prevented
then by eclosion behavior. The latter consists of waves of by mechanical contact of the insect with its surroundings
abdominal contraction and of ‘shrugging’ of the wing such as occurs while the insect is still within its old cuticle.
bases that continues until eclosion is complete. These Similar inhibition occurs in insects, such as some flies, that
movements are produced by the synchronous activity of pupate below the surface of the ground, and in first stage
muscles on the two sides of the body with activity spread- grasshoppers when they hatch from their underground
ing forwards from the posterior abdominal segments (Fig. eggs. In both cases, bursicon release is inhibited while the
400 POSTEMBRYONIC DEVELOPMENT
(pmol.h -1)
2
occurs. The small peak in juvenile
hormone production before pupation
corresponds with a second JH- 1
sensitive period, perhaps regulating
development of the imaginal discs (c, no data worker
time at which cells are capped by 0
workers) (after Rachinsky & 0 5 10
Hartfelder, 1990, and other sources). days after hatching
insects are digging, but begins as soon as they are free on hormone or ecdysone are often involved, but, in other
the surface. cases, neurosecretions from the brain provide the link
In Manduca, and probably in other insects, a cardioac- between the nervous system and the tissues.
tive peptide accelerates the pumping activity of the heart
facilitating wing expansion. Castes of social insects Amongst the social
Review: Reynolds, 1985 Hymenoptera, the queen and workers are all female. In
Apis, the newly hatched female larva has the potential to
develop into either form. Its subsequent development is
15.5 POLYPHENISM
determined by the quality and quantity of the food sup-
The term polymorphism has been used in a general sense plied to it. If given a diet based primarily on secretions of
to indicate variation in body form or color within a species. the nurse bees’ mandibular glands, it will become a queen.
It is evident, however, that, while some instances of poly- If it receives larger proportions of secretion from the hypo-
morphism are under strict genetic control, others are a pharyngeal glands of the workers, it will itself become a
product of the environment in which the insect develops. worker. Similarly, amongst the larvae of worker ants, the
These instances are now usually referred to as polyphen- differentiation of minor or major workers, or of soldiers, is
ism. Thus, polyphenism refers to the occurrence of dependent on feeding, which is ultimately reflected in the
different phenotypes within a species where the develop- sizes of the larvae.
ment of the phenotype is governed by environmental These size differences lead to different titers of juve-
conditions. nile hormone which controls the insects’ development.
Polyphenism is a characteristic feature of social insects, The switch from worker to queen in Apis is made in the
where the different castes are determined by the needs of late fourth and early fifth larval stages. Queen larvae
the colony, and of aphids, where different morphs occur develop a high titer of juvenile hormone late in the fourth
seasonally. In addition, many insects exhibit seasonal vari- larval stage, whereas in workers the titer is very low (Fig.
ations in form that can be attributed to environmental 15.35). Amongst larval ants, major worker or soldier
conditions. Different color forms, or differences in wing development is apparently the result of a high titer of
development are among the more common. juvenile hormone early in the final larval stage. If the titer
In all these cases, the environmental conditions modu- is above a threshold, the critical size at which pupation
late the amounts or timing of hormone secretion. Juvenile occurs is reset so that the larva continues to develop until
POLYPHENISM 401
a) sensitive period for the threshold for juvenile hormone that must be reached
juvenile hormone
W S
for the switch to soldier production to occur. Not only
does the high titer of juvenile hormone reset the critical
threshold raised by pheromone
size for pupation, it may also reprogram the development
juvenile hormone titer
reprogramming
(log scale)
flies to secondary
SPRING host SUMMER
fundatrigenia
crowding and
virginopara poor hostplant
fundatrix
quality
daylength
overwintering
egg
virginopara virginopara
virginopara
male
WINTER FALL
ovipara
Fig. 15.37. Polyphenism. Control of wing development and the production of sexual forms in an aphid. Seasonal changes
in form result largely from responses to long or short daylengths. The production of winged virginopara in summer is a
response to crowding or poor hostplant quality (based on Hardie & Lees, 1985).
Brachyptery in other insects Short-winged forms are Crowding the larvae of some Lepidoptera and grass-
known to occur in many species of Orthoptera and hoppers causes them to become darker, or to have more
Hemiptera. Long wings are often produced in response to dark patterning, than siblings reared in isolation. This is
crowding or poor food quality. The suppression of wing due to the deposition of greater quantities of melanin in
development is a response to high titers of juvenile the cuticle, which in caterpillars is controlled by a neuro-
hormone in final stage larvae, but experiments on crickets peptide. At least in Spodoptera littoralis, crowded larvae
indicate that this effect may be very subtle (Zera & Tanaka, have higher hemolymph titers of this neuropeptide
1996). (Altstein, Ben-Aziz & Gazit, 1994). The same peptide in
the adults controls pheromone biosynthesis (section
Color and Form Many insects exhibit color variation in 27.1.5).
response to environmental changes. These may be regular In locusts, insects reared in isolation are usually green
occurrences, as in the seasonal forms of some butterflies, with little black pigmentation; those reared in crowds are
or more unpredictable, as in the phenomenon of yellow or orange with extensive black pigmentation. The
homochromy (section 25.5.2.2). pronotum of Locusta reared in isolation is produced into
DIAPAUSE 403
15.6 DIAPAUSE
a prominent dorsal crest, while in crowded insects it is
saddle shaped. Insects reared in crowds have fewer sen- Diapause is a delay in development evolved in response to
silla on the antenna than their isolated siblings regularly recurring periods of adverse environmental
(Greenwood & Chapman, 1984). Similar changes in color conditions. It is not referable to immediately prevailing
and anatomy may occur in non-swarming grasshoppers adverse environmental conditions, and thus differs from a
and differences in an insect’s exposure to odors may delay produced by currently adverse conditions such as
affect the numbers of sensilla on the antennae, but low temperature.
whereas locusts also exhibit marked changes in behavior In temperate regions, diapause facilitates winter sur-
as a consequence of crowding, grasshoppers usually do vival; in the tropics, it is commonly associated with surviv-
not do so. The regulatory mechanisms underlying these ing regularly occurring dry seasons. Diapause also
differences are not well understood although neurosecre- contributes to the synchronization of adult emergence so
tion from the brain is known to be involved. Juvenile that the chances of finding a mate are considerably
hormone titers also differ in the final stage larvae improved. This is particularly necessary in long lived
depending on whether they are crowded or not (Pener, species such as the dragonfly, Anax, in which larval
1991). A behavioral change can occur within four hours development usually extends over two summers and
of a switch from isolation to crowding (Bouaïchi, during this time individual rates of development vary so
Roessingh & Simpson, 1995). that at any one time a wide variety of larval sizes is present.
An extreme example of polyphenism which involves
differences in morphology as well as in color occurs in the 15.6.1 Occurrence of diapause
caterpillar of Nemoria arizonaria. The spring generation Many insects living in regions where winter temperatures
of this species resembles the catkins of the oak trees on are too low for development enter a state of diapause at
which it feeds. A second generation occurs when the tree is some stage of the life history, but the occurrence of dia-
in leaf. The insects of this generation feed on the leaves pause in insects from warmer regions depends on the
and are twig mimics rather than catkin mimics. They are severity of their environment and the conditions in their
greenish-grey in color, rather than yellow, and they lack particular micro-habitat. Many insects in the tropics
many of the cuticular outgrowths which help to give survive without a diapause.
insects in the spring generation their resemblance to Diapause can occur in any stage of development from
catkins. The development of the two phenotypes is deter- the early embryo to reproductive adult, but in the majority
mined by the food eaten by the insects and, since the leaves of diapausing species, only one stage exhibits diapause
of these oaks are very tough, the insects of the summer (Fig. 15.39). Egg diapause is common in grasshoppers and
generation develop relatively larger heads (Fig. 15.38) Lepidoptera, occurring early in embryogenesis in some
(Greene, 1989). It is possible that food quality affects form species, and much later in others. Many holometabolous
404 POSTEMBRYONIC DEVELOPMENT
a) latitude b) temperature
pupae entering diapause (%)
100 100
75 75
50 43 o 50 o 60 o
50 25 o C 15 o C
25 55 o 25 30 o C
20 o C
0 0
12 14 16 18 20 22 24 12 14 16 18 20 22 24
daylength (hours) daylength (hours)
Fig. 15.41. Diapause in the moth Acronycta (after Danilevskii, 1965). (a) The effects of photoperiod. Diapause is prevented
by long days, but the critical daylength, at which the switch from non-diapause to diapause development occurs, increases
at higher latitudes. All insects were reared at 23 °C. (b) The interaction of photoperiod with temperature. The critical
photoperiod for diapause is reduced in insects reared at higher temperatures. All insects were from the same population,
from 50° N.
pupal Acronycta (Lepidoptera) and Pieris, respectively. Acronycta is about 16 hours at 25 °C, but almost 19 hours at
This number varies, however, under the influence of tem- 15 °C. (Fig. 15.41b). In Pieris, however, the critical
perature and nutrition. daylength is not influenced by temperature.
The response of many animals to photoperiod involves
Photoperiod Outside the tropics, long days occur in the perception of small changes in daylength rather than
summer and short days in winter with increasing or the actual duration of the light period, but in insects this is
decreasing daylength in spring or autumn. The relatively not the case. Most insects respond to the absolute length of
short days of autumn herald the approach of winter and the photoperiod. A few cases in which the insect is believed
for many species they act as a stimulus initiating diapause. to respond to changes in daylength are recorded, but even
There is a critical daylength around which small these can probably be accounted for in terms of reactions
differences in photoperiod produce a complete change to the absolute daylength.
from non-diapause to diapause development (Fig. 15.41). Cells in the brain are directly sensitive to light in many
As these insects develop without diapause under long-day insects, and, in these species, the compound eyes and ocelli
conditions they are known as long-day insects. do not mediate the photoperiodic response, and some-
Some insects react in the opposite way. Bombyx is an times, as in the larva of Pieris, there is a relatively transpar-
example of such a short-day insect. Here exposure of the ent area in the cuticle of the head above the sensitive area in
eggs of the bivoltine race to long days, ensures that the the brain. On the other hand, in the beetle, Pterostichus, in
eggs of the next generation will enter diapause (Fig. which the cuticle of the head is heavily pigmented, the
15.42). Adults developing from eggs exposed to a photo- compound eyes mediate the response.
period of less than 14 hours lay non-diapausing eggs in the Light intensity during the photoperiod is not important
next generation. Thus the long-day conditions of spring provided that it exceeds a very low threshold value. This
acting on the eggs lead to the production of diapause eggs varies with the species, but commonly is about 170 lux or
in the autumn, but these eggs, being subjected to short less. Hence daily fluctuations in light intensity due to
days, will ensure that the eggs of the next generation, laid clouds have no effect on photoperiod and the ‘effective
the following spring, develop without diapause. daylength’ includes the periods of twilight. As a result of
Photoperiod interacts with temperature, and in long- this high sensitivity, insects inside fruit and even the pupa
day insects the critical day-length, below which diapause of Antheraea inside its cocoon are affected by photoperiod.
occurs, is often longer at lower temperatures. For example, Some insects are so sensitive that they are stimulated by
the critical daylength inducing pupal diapause in moonlight (about 5 lux) which might, therefore, contribute
406 POSTEMBRYONIC DEVELOPMENT
does not seem to be a consequence of high juvenile hormone causes a change in pigmentation of the serosa
hormone titers. due to the uptake of 3-hydroxykynurenine which is sub-
Diapause early in embryogenesis is produced by a dia- sequently converted to an ommochrome.
pause hormone in the parent female. In Bombyx, the Adult diapause is linked to the absence of juvenile
hormone acts only on oocytes weighing about 500 g; hormone which is usually involved with vitellogenin syn-
smaller or larger oocytes are not affected. The hormone thesis or uptake (section 13.2.4.2), and, in males, with the
results in an increase in trehalase activity in the oocytes development of reproductive behavior.
leading to the conversion of hemolymph trehalose to Reviews: Danilevskii, 1965; Denlinger, 1985; Tauber, Tauber &
glycogen in the yolk (Yamashita, 1996). In addition, the Masaki, 1986
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PART IV
The integument is the outer layer of the insect, comprising The basal plasma membrane is commonly flat and
the epidermis and the cuticle. The cuticle is a character- attached to the basal lamina by hemidesmosomes, but in
istic feature of arthropods and is, to a large extent, respon- some specialized wax-secreting epithelia it forms a plasma
sible for the success of insects as terrestrial animals. membrane reticular system (section 6.1.1), and in gland
cells it is folded inwards (Fig. 16.1b).
Epidermal cells have extensive rough endoplasmic
16.1 EPIDERMIS reticulum and Golgi complexes, and they often contain
membrane-bound pigment granules.
16.1.1 Epidermal cells All the epidermal cells are glandular in the sense that
The epidermis is the outer cell layer of the insect. It is one they secrete cuticle and the enzymes concerned in its pro-
cell thick with cell densities ranging from about duction and its digestion at the time of molting. Some of
3000 mm⫺2 in a trachea of Rhodnius to 11 000 mm⫺2 in the the cells have an additional specialized glandular function,
sternal area of larval Tenebrio, but cell density and cell and these fall into three classes (Noirot & Quennedy,
depth at right angles to the surface of the epidermis 1974). Class 1 gland cells have the outer plasma membrane
change during development (see below). produced as microvilli or parallel lamellae which may abut
The apical plasma membrane of an epidermal cell directly on to the cuticle, but are often separated from it by
forms a series of short projections or ridges, flattened at a space in which it is presumed their secretion accumulates
the tips where the membrane is electron-dense on the (Fig. 16.1b). The cuticle above the cells is usually
inside (Figs. 16.1a, 16.18). These specialized regions of unmodified and it is presumed that the secretion reaches
membrane are known as plasma membrane plaques and the external surface of the cuticle via the pore canals and
they are the sites of secretion of the outer epicuticle and of epicuticular filaments. Class 1 cells are often involved in
chitin fibers. During and just after a molt, the epidermal pheromone production (section 27.1.1).
cells also have cytoplasmic processes on the outside Class 2 gland cells are derived from epidermal cells, but
extending into the pore canals of the cuticle (see Fig. 16.2), have no direct contact with the cuticle, nor do they have a
but these processes may be withdrawn as the cuticle duct. They are only known from the sternal glands of ter-
matures. mites (see Noirot & Quennedy, 1974).
The epidermal cells are held together near their apices Class 3 gland cells are also below the epidermis, but
by zonulae adhaerens and lower down by septate junctions connect with the exterior by a duct (Fig. 16.1c). The distal
(Fig. 16.1a). At greater distances from the cuticle, adjacent surface of the gland cell is developed into microvilli which
cells are not tightly bound to each other, and the spaces surround a cavity. This cavity is extracellular and therefore
between them (lateral lymph spaces) are, to some extent, is not a vacuole, although it is often referred to as such.
isolated from the hemolymph by desmosomes close to the The lining of the duct leading to the outside is continuous
basal lamina (Locke, 1991). Gap junctions between epi- with the epicuticle on the outside of the body. Internally it
dermal cells probably provide a pathway for the movement projects into the cavity of the gland cell and it is per-
of low molecular weight substances, such as hormone forated, forming a structure called the end apparatus. The
second messengers, and perhaps morphogens. This duct is produced by a separate cell.
enhances coordination between cells, reducing any minor Gland cells of this type produce the cement on the
differences that might occur due to slight differences in the outer surface of the cuticle (see below) and exhibit
timing or amounts of hormonal signals carried by the hemo- cycles of development that are synchronized with the
lymph. molting cycle (Horwath & Riddiford, 1991). In all
[415]
416 INTEGUMENT
a) epidermal cell
cuticle
zonula adhaerens
gap junction
endoplasmic
reticulum
nucleus
desmosome
basal lamina
hemidesmosomes
cuticle cuticle
microvilli
epidermal cell
duct cell
end apparatus
nucleus
cavity
basal lamina
Fig. 16.1. Epidermal cells. (a) Principal features of an epidermal cell during the intermolt period. (b) Class 1 gland cell with no
duct to the exterior (based on Noirot & Quennedey, 1974). (c) Class 3 glandular unit (based on Noirot & Quennedey, 1974).
dipterous larvae they form peristigmatic glands. These involved in the production of defensive secretions and
are composed of large cells with ducts opening to the pheromones (Chapter 27).
outside near the edges of the spiracles. Their secretion, The neurons and support cells of mechano- and
which is produced continuously, is responsible for the chemoreceptors associated with the cuticle are also derived
hydrofuge properties of the cuticle surrounding the from epidermal cells.
spiracles which prevent the entry of water into the tra- Reviews: Caveney, 1985, 1991 – cell coupling; Locke, 1984,
cheal system. In addition, class 3 gland cells are often 1985a, 1991 – ultrastructure; Noirot & Quennedy, 1974 – glands
BASIC STRUCTURE OF CUTICLE 417
b)
cement
wax
a)
outer
epicuticle
epicuticle
inner
epicuticle
exocuticle
wax canal
pore canal filament
endocuticle
Schmidt's
layer
epidermis exocuticle
basal lamina pore canal
Fig. 16.2. Basic structure of the integument: (a) section through mature integument; (b) section through the epicuticle at
greater magnification.
b) CHAIN C CHAIN D
CH 3
hydrogen C
bond O N O
hydrogen
H bond
O
H
O CH 3
O N OH
H bond to C C H bond to
chain OH O N O chain
CH 3
A H E
O O
H H bond to
O N O CH 3 chain
HO
C C F
HO
CH 3 O N O
H
O
O
H
O H bond to
O N chain CH 3
C OH
B C
OH CH 3 O N O
H
cuticle, while proteins produced by another gene family Hardening of cuticle is primarily a consequence of
characterize hard cuticle. These differences are apparent cross-links between protein molecules so that they form a
even before the cuticle is hardened, and the differing phys- rigid matrix. The process of cross-linking is called tanning
ical properties of different parts of the cuticle appear to be or sclerotization and the cuticle is then said to be sclero-
at least partly a consequence of the different proteins they tized (see below, section 16.5.3).
contain, independent of the hardening process. The pro- Reviews: Andersen, Højrup & Roepstorff, 1995; Willis, 1987,
teins of soft cuticle generally contain more aspartic acid, 1991
glutamic acid, histidine, lysine and tyrosine and are more
hydrophilic than those of hard cuticles. The same proteins 16.2.1.3 Lipid
are present in cuticle with similar properties from different Lipids are present in the procuticle and, in Rhodnius, they
stages of an insect: the proteins appear to characterize the impregnate the walls of the pore canals and are present in
type of cuticle rather than the stage of development. layers at intervals of 0.5–1.0 m. These lipid layers become
420 INTEGUMENT
a)
1
2
3 ................................................................. one
1 7 5
4
lamella
6
7
2 6
3 5
4
b)
1
2
3
4 fibrils parallel to
5
6
plane of section
7
8
9
10
1-9 15-23
11
13
12 ................................................................. fibrils at right angles
15
14 to plane of section
16
17
18
19
10 14 20
21
22
23
11 13
12
1
2
c) 3
4
5
6
7
8
9
10
fibrils oblique to
11
12 .................................................................
................................................................. plane of section
13
14 .................................................................
.................................................................
15 ................................................................. fibrils at right angles
1-9 23-31 17
16 .................................................................
................................................................. to plane of section
19
18 .................................................................
.................................................................
20
21
22
10 22 23
24
25
26
27
11 21 28
29
12-20 31
30
Fig. 16.4. Diagrams showing the arrangement of chitin microfibrils in cuticle. Numbers indicate successive layers in the
cuticle with (left) the orientation of microfibrils in successive layers as seen in transparency through the cuticle, and (right)
the appearance of the fibrils in sections of the cuticle running parallel with the fibrils in layer 1. (a) A helicoidal arrangement
producing a single lamella. (b) Two layers with uniformly oriented microfibrils (1–9 and 15–23) separated by a single lamella
with a helicoidal arrangement (10–14). (c) Layers of uniformly directed fibrils at right angles to each other (1–9, 12–20 and
23–31) separated by layers with a helicoidal arrangement (10–11 and 21–22).
dispersed when the insect feeds and the cuticle stretches, but epicuticle, only about 15 nm thick, and outside this again is
more layers are laid down with the new cuticle. Wigglesworth a wax layer of variable thickness. Some insects have a thin
(1988) believes that lipid, together with the sclerotized pro- ‘cement’ layer outside the wax (Fig. 16.2b).
teins, plays a significant role in cuticle hardening.
Inner epicuticle This layer is chemically complex and is
16.2.2 Epicuticle known to consist primarily of tanned lipoproteins. During
The epicuticle is made up of several layers. The thickest its production, phenolic substances and phenoloxidase are
layer, 0.5 to 2.0 m thick, is the inner epicuticle immedi- also present. These are probably concerned with tanning
ately outside the procuticle. Outside it, is a very thin outer the proteins. Phenoloxidase persists as an extracellular
BASIC STRUCTURE OF CUTICLE 421
0 20 40 60 0 20 40 60 0 20 40
hydrocarbons
wax esters
free fatty acids
alcohols
triacylglycerides
sterols
others
0 20 40 60 0 20 40 60 0 20 40
% % %
d) chain lengths
(values of x)
CH 2 - O - fatty acid
CH 2 - O - fatty acid
sterols -
HO
Fig. 16.5. The main groups of compounds occurring in epicuticular wax shown as percentages of the total wax: (a) a
grasshopper – hydrocarbons predominate; (b) a caterpillar – alcohols predominate; (c) an adult stonefly – free fatty acids
predominate; (d) the structures of the main types of compound. Chain lengths are shown in the final column, where
appropriate. These values refer to X in the previous column.
enzyme in mature cuticle, producing further tanning if the limit on any extension of the procuticle during growth or
epicuticle is damaged. other activities. The material forming the outer epicuticle
is often referred to as cuticulin.
Outer epicuticle This is a very thin trilaminar layer. It is a
highly polymerized lipid, and probably also has a protein Wax The epicuticular wax layer contains many different
component. Polyphenols and phenoloxidase take part in its compounds (Fig. 16.5). Hydrocarbons are universally
formation. It is the first-formed layer of new cuticle pro- present, and may comprise over 90% of the wax, as in the
duced at each molt, protecting the new procuticle from the cockroaches. Chain lengths range from around 12 to over
molting enzymes. It is believed to be inextensible, setting a 50 carbon atoms, and compounds with an odd number of
422 INTEGUMENT
carbon atoms in the chain are usually dominant. In larval 16.2.3 Pore canals and epicuticular filaments
Lepidoptera and Coleoptera, aliphatic alcohols are the Running through the cuticle at right angles to the surface
most abundant compounds. In this case, compounds with are very fine pore canals one micron or less in diameter
even numbers of carbon atoms, in the range 12 to 34, are (Fig. 16.2b). They extend from the epidermis to the inner
dominant. The alcohols may form esters with fatty acids, epicuticle and, at least early in the development of the
but esters are usually only minor components. In an adult cuticle, contain cytoplasmic extensions of the epidermal
stonefly, free fatty acids constitute the principal class of cell at densities as high as 15000 mm⫺2. In adult beetles
compounds in the wax. and bugs the pore canals are more abundant in the outer
It has been suggested that the molecules adjacent to the procuticle, and some 30 pore canals per cell in the outer
outer epicuticle are strongly oriented as a result of their region may join to a single canal lower down.
polar, hydrophilic groups being adsorbed on to the surface In Rhodnius, the pore canals are circular in cross-
of the cuticulin so that they form a layer only one molecule section, but in many species they have a flattened,
thick and hence called a monolayer. However, current evi- ribbon-like form, the plane of flattening being parallel
dence does not support this idea (section 18.4.1). with the microfibers in each layer of the cuticle. As the
In some species, the wax forms a bloom on the outside microfibers in successive layers change direction the
of the cuticle and, in a few, very large quantities are pro- canal also rotates, so that it has the form of a twisted
duced. This is the case with some Fulgoroidea and scale ribbon (Fig. 16.6).
insects, and the larva of Calpodes. Bees secrete large quanti- It is presumed that the cytoplasmic threads within the
ties of wax, which they use in the production of their larval canals are subsequently withdrawn and the canals may be
cells. This wax is secreted by epidermal cells on the ventral filled by chitin and protein with the chitin microfibers ori-
surface of abdominal segments four to seven. These cells ented along the canal. Whether they are filled or not, the
presumably contribute to the insect’s epicuticular wax, but canals contain tubular filaments (called wax canal
they become greatly enlarged when the bees have an ade- filaments, or epicuticular filaments) arising from the
quate supply of honey which provides the basic chemicals plasma membrane of the epidermal cell. At the epicuticle,
from which the wax is produced. The secretion of the these filaments diverge and extend to the surface of the
glands, which contains over 300 components, is pressed outer epicuticle (Fig. 16.2b). The filaments range from
into flat scales between the overlapping sterna. The scales 13 to 21 nm in external diameter in different insects, and
are removed by spines on the posterior basitarsi and are have a lipid-filled lumen of about half this diameter. They
manipulated with the forelegs and mandibles to produce possibly consist of tanned protein and are concerned with
the cells of honeycomb (Winston, 1987). the transport of lipids from the epidermal cells to the
The wax is important in waterproofing the cuticle surface of the cuticle (Wigglesworth, 1985).
(section 18.4.1.1) and, in some insects, is the source of
chemical signals important in intra- and, perhaps,
16.3 DIFFERENT TYPES OF CUTICLE
interspecific signalling. It is synthesized by the oenocytes.
Reviews: Blomquist & Dillwith, 1985; de Renobales, Nelson & The cuticle varies in nature in different parts of the body
Blomquist, 1991; Lockey, 1988 and between insects with different life forms. The most
obvious difference is between the rigid cuticle of the scle-
Cement The cement is a very thin layer outside most of rites and the flexible cuticle of the membranes between
the wax, perhaps consisting of mucopolysaccharide which them.
becomes closely associated with lipids. It may serve to
protect the underlying wax, although it is sometimes 16.3.1 Rigid and hard cuticle
present as an open meshwork. It is not produced by all Rigid cuticle is produced as a result of sclerotization in the
insects and appears to be absent from the cuticle of honey- outer part of the procuticle to form exocuticle and its
bees, for example. stiffness increases as a greater proportion of the cuticular
Cement is the product of type 3 gland cells in the epi- proteins become cross-linked (Fig. 16.7). The extent of
dermis. sclerotization varies between different developmental
Review: Horwath & Riddiford, 1991 stages and in different parts of the cuticle. In larval
DIFFERENT TYPES OF CUTICLE 423
eclosion 0 2 4 6
pharate
adult
adult mandible
100 10
elastic modulus (MPa x 100)
hind tibia
sclerotized cuticle (%)
hind femur
75 head capsule
mesonotum
50 5 mesopleuron
sclerotized
cuticular cuticle pronotum
larva
25 stiffness mesosternum
abdominal sclerite no data adult
3 5 10 (abdominal)
days 0 2 4 6
relative sclerotization
Fig. 16.7. The relationship between sclerotization and cuticular
stiffness. Over the period of the molt, and principally around the Fig. 16.8. Amounts of sclerotization of the cuticle from different
time of eclosion, the degree of sclerotization of an abdominal parts of the body of a mid fifth-stage larva and a 10-day-old adult
tergite of the honeybee increases. (Sclerotization is expressed as locust. Sclerotization is based on the amounts of ketocatechols
the inverse of the percentage of protein that is extractable. Only released when the cuticle is hydrolysed (based on Andersen,
about half the protein in the cuticle becomes bound). At the same 1974).
time, the stiffness of the cuticle, measured as the elastic modulus,
also increases (based on Richards, 1967). dorsal mesothorax is particularly heavily sclerotized in
relation to its function in flight (Fig. 16.8).
Schistocerca, for example, the exocuticle of the sclerites is Additional rigidity is produced in sclerotized cuticle by
sharply differentiated from the endocuticle, which never structural modifications. These are based on inflexions of
sclerotizes. In the adult, on the other hand, some changes the cuticle seen as grooves (sulci) on the outside and as
continue for weeks after the final ecdysis and the whole of ridges on the inside. Most of the grooves seen in insect
the procuticle may become differentiated. In the fully cuticle and which define the areas of cuticle given specific
hardened larva of Schistocerca, the mandibles are much names by morphologists are formed in this way. These
more heavily sclerotized than other parts of the cuticle; inflexions provide rigidity in the same way as a T-girder.
they are also heavily sclerotized in the adult, but to no Even greater rigidity is provided when inflexions meet
greater degree than some other parts of the body. The internally to form an ‘internal’ (endophragmal) skeleton.
424 INTEGUMENT
Deep, finger-like invaginations of the cuticle are called beetles (Leschen & Cutler, 1994), but it is not usually a
apodemes or apophyses. In the head, four apodemes join significant component of insect cuticle.
centrally to form the tentorium (see Fig. 1.5), and in the
thorax of winged insects, pleural and sternal apophyses 16.3.2 Membranous cuticle
join or are held together by muscles (see Fig. 7.4). The The sclerites are joined by flexible arthrodial membranes.
tentorium provides rigidity to the head just above the level In these, the procuticle remains unsclerotized (Fig.
at which the mandibles are articulated. The junction of 16.10a), but it also differs qualitatively from the cuticle of
pleural and sternal apophyses gives lateral stiffness to the sclerites in containing proteins with different amino acid
thorax which is important for the proper functioning of composition. The extent of the membrane and the method
the flight muscles. of articulation of the two adjacent sclerites determines the
Hardness, as opposed to rigidity, increases relatively degree of movement that can occur at the joint.
slowly after ecdysis and it may take several days for the Sometimes, as between abdominal segments, the mem-
cuticle to reach its final degree of hardness. During this brane is extensive and there is no specific point of contact
time, the cuticle increases in thickness and this may between adjacent sclerites, so that movement is unre-
contribute to the increased hardness (Hillerton, Reynolds stricted (Fig. 16.10a, b). More usually, the sclerites make
& Vincent, 1982). It may also be that other changes occur contact with each other to form articulations and the joints
in the cuticle following the initial rapid sclerotization. are called monocondylic or dicondylic depending on
Parts of the cuticle that are especially hard contain whether there are one or two points of contact (see Fig.
heavy metals. Zinc, manganese, or occasionally iron, are 8.1). Monocondylic articulations, such as that of the
present in the mandibles of insects with biting and antenna with the head, permit considerable freedom of
chewing mouthparts from several orders (Fig. 16.9). movement, whereas dicondylic articulations, which occur
These metals are present in relatively large amounts, com- at many of the leg joints, give more limited, but more
prising considerably more than 1% of the dry weight of precise movements, and a less complex array of muscles is
the cuticle in which they occur. These metals are also necessary to provide fine control of movement. The artic-
present in the claws and ovipositors of some insects. Their ular surfaces may lie within the membrane (intrinsic), as in
role in hardening is inferred from their presence in areas most leg joints (Fig. 16.10c, d), or they may lie outside it
which are known to be especially hard, but the mechanism (extrinsic), as, for example, in the mandibular articulations
by which they produce hardness is not known (Chapman, (Fig. 16.10e).
1995). Apart from membranous areas, exocuticle is also absent
Calcium, probably as calcium carbonate, possibly along the ecdysial cleavage lines of larval hemimetabolous
contributes to cuticular hardness in some tenebrionid insects. The cuticle along these lines consists only of
DIFFERENT TYPES OF CUTICLE 425
a) b) membrane
sclerite sclerite
sclerite epicuticle
exocuticle
membranous
cuticle
c) d) e)
sclerotized
cuticle sclerotized
cuticle
sclerotized cuticle
of head capsule
membranous
cuticle
sclerotized cuticle
membranous of mandible
cuticle
Fig. 16.10. Flexibility of the cuticle. Arrows show points of articulation at which the two sclerotized regions meet and are free
to move relative to each other (partly after Snodgrass, 1935). (a) Intersegmental membrane. Extensive membrane with no
articulation between sclerites. (b) Diagrammatic representation of a membranous connection similar to that in (a). (c) An
intrinsic articulation where the points of articulation are within the membrane, as in most leg joints. (d) Detail of one of the
articulations in (c). (e) Extrinsic articulations where the sclerotized parts meet outside the membrane.
fibrous
pleuron protein
Plasticization of cuticle Whereas resilin is an elastic the blowfly, Calliphora, plasticization of the sclerites
protein, undifferentiated procuticle can sometimes be occurs when the newly eclosed fly swallows air and pumps
plasticized in order to facilitate stretching. This probably rhythmically to expand the cuticle. Very little extension of
occurs in all insects at the time of ecdysis, where plasticiza- the cuticle can be produced before this period even though
tion facilitates expansion of the new cuticle. It also occurs the procuticle is still undifferentiated. Once sclerotization
in the blood-sucking bug, Rhodnius, during feeding, and in begins, the cuticle is again inextensible (Fig. 16.13).
female grasshoppers when ovipositing. In Manduca, and probably in other insects, these
Plasticization at ecdysis facilitates the stretching of changes are regulated by two hormones, eclosion
presumptive sclerites, before the cuticle is sclerotized. In hormone, which is released into the hemolymph just
MOLTING 427
molt intermolt
Fig. 16.14. The sequence of events involved in cuticle production. The timing of apolysis and the degree of overlap between
procuticle production and cell division vary from species to species.
before ecdysis and which also switches on ecdysis behavior, Female locusts and grasshoppers lay their eggs in the
and bursicon, which is released just after eclosion and ground, often extending the abdomen to more than twice
which subsequently initiates sclerotization. its normal length by stretching some of the intersegmental
Rhodnius larvae normally take only one very large blood membranes (see section 13.5.2). The membranes are not
meal in each developmental stage. This results in consid- extensible in males.
erable distension of the abdomen, so that its surface area Review: Reynolds, 1985
increases about fourfold and the cuticle becomes consider-
ably thinner. This distension is facilitated by plasticization
16.4 MOLTING
of the largely unsclerotized abdominal cuticle.
Plasticization is apparent within two minutes of the start of Growth is limited by the cuticle. Sclerotized cuticle is vir-
feeding, and is initiated by the pumping activity associated tually inextensible, and membranous cuticle can stretch
with food intake. Information is passed via stretch recep- only to the extent that folds in the outer epicuticle allow.
tors to the central nervous system from which neuro- As a result, for any marked increase in size to occur, the
secretory axons extend to the body wall where they branch cuticle must be shed and replaced. Casting the cuticle is
extensively beneath the epidermis. They release serotonin commonly known as molting, but it involves a sequence of
so that a high local concentration occurs (Orchard, Lange events beginning with the separation of the old cuticle
& Barrett, 1988). from the underlying epidermal cells and ending with the
The cuticle in the plasticized regions contains only remnants of the old cuticle being shed. These processes
about 11% chitin, and the constituent proteins are low in are known as apolysis and ecdysis, respectively. After
aspartic and glutamic acids, but high in alanine and histi- ecdysis, the new cuticle is expanded and chemically
dine. The low levels of amino acids with bulky side-chains modified. In most insects, extensive deposition of new
may facilitate sliding of the protein molecules. As the cuticle continues in the intermolt period. The timing of
cuticle is unsclerotized, the molecules are held together by events is illustrated in Fig. 16.14 and changes in the
relatively labile bonds; it is believed that a change in pH integument in Fig. 16.17. The hormonal regulation of
within the cuticle disrupts the bonding. molting is discussed in section 15.4.
The increase in abdominal size in Rhodnius associated
with plasticization is to a large extent reversible and the 16.4.1 Changes in the epidermis
abdomen slowly shrinks to approach its original size as the In most insects with well-sclerotized cuticles, such as the
blood meal is digested and excess fluid is excreted larvae of most hemimetabolous insects, epidermal cell
(Reynolds, 1985). density is constant through most of the intermolt period.
428 INTEGUMENT
Fig. 16.15. Changes in the density or size of epidermal cells in relation to molting. Expansion and cell destruction decrease
cell density; cell division increases it. (a) Tracheal epithelium of larval Rhodnius. A similar pattern probably occurs in
epidermis associated with sclerites in other insects except for the expansion due to feeding (based on Locke, 1964). (b)
Epidermis of larval Manduca, an example of an insect with unsclerotized cuticle (data from Wielgus & Gilbert, 1978). (c) In
cyclorrhaphan Diptera no cell division occurs in the larval epidermis. Increase in epidermal area is entirely dependent on an
increase in cell size. At the same time the DNA content of the nuclei increases due to endomitosis and the nuclei increase in
volume (after Pearson, 1974).
It increases as a result of mitosis at the onset of the molting the cells spread laterally (Fig. 16.15b). Then, when mitosis
cycle and then undergoes a sharp, relatively small decrease occurs and the number of cells is increased, cell density
during cuticular expansion following ecdysis (Fig. 16.15a). increases sharply. At the larval–pupal molt, some increase
There is a net increase in the total number of cells so that in density probably also occurs due to rearrangement of
although the number per unit area returns to its original the cells as the larva shortens. Cell growth in the period
value, the overall area of the epidermis, and hence of the before ecdysis results in a subsequent decrease in density.
cuticle which it produces, is increased. In larval forms with These changes in epidermal cell density are accompa-
flexible cuticle, however, the pattern of changes is nied by changes in cell shape. In Rhodnius, the cells are
different. In the period of feeding following ecdysis, cell columnar immediately after molting, but then become
density decreases as the cuticle above the cells unfolds and squamous until the insect feeds; after this they become
MOLTING 429
a) b)
c) d)
e) f)
Fig. 16.16. Changes in the shape of epidermal cells during the final larval stage of Calpodes (Lepidoptera) (after Locke,
1985b): (a) 36 hours after ecdysis from the fourth stage; (b) 72 hours after ecdysis. Cell growth keeps pace with the increasing
size of the larva; (c) the larva has reached its maximum size and the cell has extensive feet; (d) the feet begin to shorten as the
larva shortens in the period before pupation; (e) cell area and the extent of feet is greatly reduced as shortening continues, but
cell depth increases as the cells become crowded; (f) about 20 hours before ecdysis to the pupa.
deeper again. The epidermal cells of caterpillars, in con- density decreases and the area of each cell increases
trast, become progressively deeper in the days following throughout larval life as it grows (Fig. 16.15c).
ecdysis, but get markedly deeper at the time of cell divi-
sion and when the insect shortens prior to pupation (Fig. 16.4.2 Separation of the cuticle from the epidermis
16.16). Before this phase, in the final larval stage of (Apolysis)
Calpodes (Lepidoptera), the cells develop basal processes, Perhaps as a result of the changes in cell shape, tension is
or feet, which become longer as ecdysteroid titer rises, generated at the epidermal cell surface resulting in its separa-
but then shorten rapidly as the larval segments also tion from the cuticle (Fig. 16.17b). In Podura (Collembola),
shorten prior to pupation. The feet are probably critically however, the outer plasma membrane of the epidermal cells
important in producing changes in the shape of an insect forms small outpushings that separate off as vesicles to form a
at a metamorphosis, and are probably formed in all foam which lifts off the cuticle. The separation of the cuticle
insects. from the underlying epidermis is known as apolysis, and the
Larval Cyclorrhapha differ from other insects because space formed between the epidermis and cuticle is called the
no cell division occurs in the epidermis. As a result, cell exuvial, or subcuticular space.
430 INTEGUMENT
endocuticle
exuvial space
endocuticle -
partially digested
molting fluid -
active
molting fluid - ecdysial
inactive membrane
new epicuticle new procuticle
oenocyte -
discharged
old exocuticle
ecdysial
membrane
undifferentiated
procuticle
Fig. 16.17. Changes in the integument over a molt. (a) Mature cuticle. (b) Apolysis follows cell division and the change in cell
shape. (c) Molting fluid is produced. At first, the enzymes it contains are inactive. The new outer and inner epicuticles are
produced. (d) The enzymes in the molting fluid are activated and start to digest the old endocuticle. At the same time new
procuticle is laid down. (e) All the old endocuticle is digested and resorbed. New procuticle becomes thicker. (f) After ecdysis
the new cuticle expands and the epidermal cells change shape. The procuticle is still undifferentiated.
MOLTING 431
16.4.3 Digestion of the old endocuticle integument (Cornell & Pan, 1983). As a result, up to 90% of
Before the cuticle is shed, the endocuticle is digested by the materials present in the cuticle may be conserved.
enzymes secreted by the epidermal cells. A mixture of As a result of the activity of molting fluid, the cuticle
enzymes is involved, including chitinases, a trypsin-like pro- becomes very thin and weak along the ecdysial lines (Fig.
tease and an aminopeptidase (Samuels & Paterson, 1996). 16.11). These vary in position, but in the locust there is a
At least in some species, some of the enzymes are ⌳-shaped line on the head (see Fig. 1.3a) and a median
present in the cuticle even before apolysis. For example, in dorsal line on the prothorax.
the larva of Calpodes, electron-dense droplets are secreted Review: Reynolds & Samuels, 1996
during the production of the last layers of procuticle.
These exuvial droplets are probably inactive precursors of 16.4.4 Ecdysis
molting enzymes. In Manduca larva, chitinase is present in When the molting fluid and the products of digestion of the
the cuticle (Bade, 1974). In many species, however, the molting fluid are resorbed, the old cuticle consists of little
enzymes are secreted into the exuvial space after apolysis. more than epicuticle and exocuticle and is quite separate
In Podura, they are produced as granules, and in various from the new cuticle (Fig. 16.17e). Ecdysis usually follows
Lepidoptera they are described as forming a gel. as soon as digestion is complete (section 15.2).
These enzymes do not start to digest the endocuticle A phase of preparatory activity loosens the old cuticle
until the outer epicuticle of the new cuticle is formed. (pre-ecdysis behavior, Fig. 15.34). It consists of a sequence
They may be inactive because they are in the form of a pre- of relatively simple motor activities following each other in
cursor (zymogen) that requires activation, or because their a more or less definite order. Carlson (1977) recognizes
substrate is not available to them. Proteolytic enzymes are seven motor programs in the preparatory phase of
probably secreted as precursors and require the secretion Teleogryllus. Adult Lepidoptera make partial rotatory
of a zymogen-activating enzyme before they become movements of the abdomen to free the themselves from
active. Chitinases, however, appear to have the potential to the pupal cuticle just before eclosion. The sequence of
be active from the time of secretion, but depend on the activities is controlled largely endogenously by the central
prior action of proteolytic enzymes that free the chitin nervous system (section 15.4.3), but feedback from
from its close association with proteins (Samuels & peripheral sensilla can prolong activities.
Reynolds, 1993). In Manduca, and probably in other The insect splits the old cuticle by exerting pressure
insects, a chitinase attacks internal linkages in the chitin against it from within. An increase in blood volume, occur-
molecule, producing small oligosaccharides. These are ring before ecdysis in Schistocerca (Fig. 5.14) and probably
then broken down by a -N-acetylglucosaminidase. The in other insects, contributes to the insect’s ability to do
two enzymes act synergistically. this. Then, in the preparatory phase of ecdysis, it usually
Activation is associated with the active transport of swallows air or water, swelling the gut so that hemolymph
potassium into the exuvial space accompanied by a bulk pressure is increased. Blood is pumped into a particular
flow of water. The fluid produced is called molting fluid part of the body, often the thorax, so that this expands and
and its ionic composition may serve to buffer the enzyme exerts pressure on the old cuticle causing it to split along
systems against pH changes during the subsequent diges- its lines of weakness. Special muscles may be concerned in
tion of cuticle, as well as contributing to the solution of these pumping movements (section 10.2.4).
exuvial droplets. When the old cuticle is split, the insect draws itself out,
The enzymes digest all the unsclerotized cuticle except usually head and thorax first, followed by the abdomen and
the ecdysial membrane (see below), but have no effect on appendages. Many insects suspend themselves freely from
the exocuticle or on the muscle and nerve connections to a support so that emergence is aided by gravity. All the cut-
the old cuticle. These connections persist so that the insect icular parts are shed, including the intima of fore- and
is still able to move and receive stimuli from the environ- hind-gut, the endophragmal skeleton and the linings of
ment, but they are finally broken at ecdysis by the move- the tracheae except for some delicate parts which may
ments of the insect. break off. The old cuticle is referred to as the exuviae.
The products of cuticular digestion are absorbed through Immediately after emergence, the new cuticle is unex-
the mouth and anus, and possibly also directly through the panded and soft, so that it provides the insect with little
432 INTEGUMENT
a) tyrosine storage takes place primarily in the epidermis, although the prod-
ecdysis ecdysis
ucts may be returned briefly to the hemolymph. The first
steps are its conversion to dihydroxyphenylalanine (dopa)
and then decarboxylation to dopamine (Fig. 16.20). From
10
this, N-acetyldopamine and N--alanyldopamine, the two
concentration (mg.g -1 )
tyrosine
b) catecholamines
hemolymph concentration (mM)
3 N-β-alanyldopamine
1 N -acetyldopamine
0
0 1 2 3 4 5 6 7 8 9 1
days
side chain of the quinone to the protein. The former is form melanin. It is probably generally true that, as in
known as quinone tanning, the latter as -sclerotization or Schistocerca, only procuticle produced before ecdysis is scle-
quinone methide sclerotization. rotized in larval insects. Procuticle which is produced sub-
sequently remains undifferentiated, so that the insects come
OH OH to have distinct exo- and endocuticles. In the adult locust,
OH OH however, where cuticle deposition continues for more than
20 days, sclerotization continues for a similar period and so
protein protein the whole thickness of the cuticle of the sclerites becomes
CH 2 protein C protein stabilized. In the larva N-acetyldopamine is produced by
H C NHCO CH 3 H C NHCO CH 3
the epidermal cells only for the first day after ecdysis,
whereas in the adult it is formed continuously. This control
H H
is effected by hemocytes, which take up tyrosine from the
quinone tanning β - sclerotization hemolymph for a limited period at the larval molt.
Membranous regions remain unsclerotized and it is
-sclerotization produces a colorless cuticle, but quinone clear that the extent of sclerotization is regulated by epi-
tanning causes the cuticle to darken. dermal cells responsible for producing the structural pro-
Most of the amino groups in the proteins are already teins and enzymes of the cuticle.
involved in the peptide linkages, -CO.NH-, between adja- Reviews: Andersen, 1985, 1991; Hopkins & Kramer, 1992;
cent amino acids forming the protein chain. Consequently, Lipke, Sugumaran & Henzel, 1983 – Diptera; Sugumaran, 1991
the only amino groups available for linking to quinones are
the terminal groups of the chains and those associated with
16.6 EXPANSION OF THE NEW CUTICLE
dibasic acids, usually lysine. In the dibasic acids only one of
the amino groups is involved in a peptide linkage, leaving In the later stages of ecdysis and immediately afterwards,
the other available for cross-linking. the insect expands the new cuticle before it hardens. This
As the cuticle hardens, it usually also darkens. This often involves swallowing air or water. In the blowfly, air is
darkening may simply result from quinone tanning, but it pumped into the gut by the pharyngeal muscles, pro-
may also involve the polymerization of excess quinones to ducing a steady increase in blood pressure (Fig. 16.21),
CHANGES IN THE INTERMOLT CUTICLE 435
a)
b)
1 m
c)
1 m
Fig. 16.22. Expansion of the new cuticle in a first stage larva of a grasshopper immediately after hatching. Similar changes
occur at subsequent molts. Left: before ecdysis of the embryonic cuticle, the larval cuticle exhibits both macro- and micro-
folds; right: after expansion, about 30 minutes later, but before sclerotization is evident. The cuticle is flat without
macrofolds and microfolds have almost disappeared. Outlines of the underlying epidermal cells producing each patch of
cuticle are clearly seen (after Bernays, 1972 and courtesy Dr E.A. Bernays). (a) Diagrammatic sections through the
integument. (b) Low power scanning electron micrographs of the surface of the cuticle. (c) Higher power scanning electron
micrographs of the cuticle.
CHANGES IN THE INTERMOLT CUTICLE 437
a) larval procuticle Fig. 16.23. Cuticular changes in the intermolt period. (a)
Changes in the thickness of the cuticle during the final larval
ecdysis wandering stage of a caterpillar (Manduca). During the period of feeding,
300 the cuticle thickens although the caterpillar is also increasing in
surface area at the same time. This is due to the continuous
pre-ecdysial cuticle
and growth
production
200 larva stage, but the cuticle becomes thicker as the larva shortens prior
shortens
to pupation (based on Wolfgang & Riddiford, 1987). (b) Changes
in the amount of cuticular hydrocarbons during the pupal and
100 early adult stages of a moth (Trichoplusia). Additional
hydrocarbon is deposited on the surface of the cuticle during the
first half of the pupal period; subsequently it remains constant.
0
This material is lost at ecdysis and a new layer of wax forms on
-2 0 2 4 6
the adult cuticle. The quantity of hydrocarbon increases sharply
days relative to ecdysis
at ecdysis and continues to rise in the following hours (based on
de Renobales et al., 1988).
b) pupal wax
ecdysis
30
weight of lipid (µg)
adult
20
pupa
10
0
0 50 100 150 200
time (hours)
new lamellae
added
microfibers of
new cuticle
plasma membrane
plaques
438 INTEGUMENT
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Reynolds, S.E. & Samuels, R.I. (1996). Snodgrass, R.E. (1935). The principles of Willis, J.H. (1991). The epidermis and
Physiology and biochemistry of insect Insect Morphology. New York: metamorphosis. In Physiology of the
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colours in insects. Zoologische Binnington & A. Retnakaran, pp. Honey Bee. Cambridge, Massachusetts:
Jahrbücher. Abteilung für Anatomie und 141–68. Melbourne: CSIRO. Harvard University Press.
Ontogenie der Tiere, 84, 25–62. Wigglesworth, V.B. (1985). The transfer Wolfgang, W.J. & Riddiford, L.M. (1981).
Romer, F. & Bressel, H.U. (1994). of lipid in insects from the epidermal Cuticular morphogenesis during
Secretion and metabolism of ecdyster- cells to the cuticle. Tissue & Cell, 17, continuous growth of the final instar
oids by oenocyte-fat body complexes 249–65. larva of a moth. Tissue & Cell, 13,
(OEFC) in adult males of Gryllus Wigglesworth, V.B. (1988). The source of 757–72.
bimaculatus DeG (Insecta). Zeitschrift lipids and polyphenols for the insect Wolfgang, W.J. & Riddiford, L.M. (1987).
für Naturforschung C 49, 871–80. cuticle: the role of the fat body, oeno- Cuticular mechanics during larval
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17 Gaseous exchange
Gaseous exchange in insects occurs through a system of absent or poorly developed and often irregularly
internal tubes, the tracheal system, the finer branches of arranged. Consequently, the airsacs collapse under pres-
which extend to all parts of the body and may become sure and they play a very important part in ventilation of
functionally intracellular in muscle fibers. Thus oxygen is the tracheal system as well as having other functions.
carried directly to its sites of utilization and the blood is Airsacs are widely distributed along the main tracheal
not concerned with its transport. In terrestrial insects and trunks of many insects.
some aquatic species, the tracheae open to the outside
through segmental pores, the spiracles, which generally 17.1.2 Tracheoles
have some closing mechanism reducing water loss from At various points along their length, especially distally, the
the respiratory surfaces. Other aquatic species have no tracheae give rise to finer tubes, the tracheoles. There is no
functional spiracles, and gaseous exchange with the water sharp distinction between tracheae and tracheoles, but the
involves arrays of tracheae close beneath the surface of latter always appear to be intracellular and often retain
thin, permeable cuticle. their cuticular lining at molting, which is not usually true
Reviews: Grassé, 1976 – general; Mill, 1985 – general; Miller, of tracheae. Proximally the tracheoles are about 1 m in
1981a – cockroaches diameter, tapering to about 0.1 m or less. They are
formed in cells (often called tracheoblasts, but
Wigglesworth, 1983, suggests the term ‘tracheolar cells’)
17.1 TRACHEAL SYSTEM which are derived from the epidermal cells lining the tra-
cheae (Fig. 17.2). It is not certain if the tracheoles develop
17.1.1 Tracheae as truly intracellular structures or if they are really extra-
The tracheae are the larger tubes of the tracheal system, cellular, forming in a deep fold of the plasma membrane of
running inward from the spiracles and usually breaking up the tracheolar cell and so having the appearance of being
into finer branches, the smallest of which are about 2 m in intracellular (Whitten, 1972; Wigglesworth, 1983). The
diameter. Tracheae are formed by invaginations of the ecto- intima of tracheoles is some 16–20 nm thick and may
derm and so are lined by a cuticular intima which is continu- consist only of outer epicuticle. It is thrown into taenidial
ous with the rest of the cuticle. A spiral thickening of the ridges, but, unlike the taenidia of tracheae, these ridges are
intima runs along each tube, each ring of the spiral being not filled with chitin/protein matrix (Edwards, Ruska &
called a taenidium (Fig. 17.1). The intima consists of outer Harven, 1958).
epicuticle with a protein/chitin layer beneath it. In the The tracheoles are intimately associated with the
taenidia the protein/chitin cuticle is differentiated as meso- tissues and, in some flight muscles, they indent the muscle
cuticle or exocuticle. The chitin microfibrils in the taenidia plasma membrane and penetrate deep into the fiber (Fig.
run round the trachea, while between the taenidia they are 17.1c,d), but it is probable that they never become truly
parallel with the long axis of the trachea. A layer of resilin intracellular within the muscle. Each tracheolar branch
may be present beneath the epicuticle (Whitten, 1972). ends blindly; there is no good evidence that they anasto-
The taenidia prevent collapse of the trachea if pressure mose to form a network, although this is described in some
within the tube is reduced. In the wing tracheae of some earlier literature.
insects, the taenidia are themselves twisted, giving some Wigglesworth (1990b) describes tracheae in the
elasticity to the wall of the trachea (section 5.1.2.1). abdomen of Calliphora in which the cuticle between the
In places, the tracheae are expanded to form thin- taenidia bulges outward having the appearance of a trache-
walled airsacs (see Fig. 17.4) in which the taenidia are ole wound round the trachea in a spiral, but with the length
[441]
442 GASEOUS EXCHANGE
a) c)
tracheole
tracheole
tracheal
epithelial cell
tracheolar
cell
trachea with
taenidia mitochondrion
muscle
fiber
d)
plasma membranes plasma membrane
b) of tracheolar cell of muscle cell
Fig. 17.1. Tracheal system. (a) Diagram showing a trachea and tracheoles. (b) Longitudinal section of the tracheal wall.
Tracheal lumen above, hemolymph below. (c) Diagram showing tracheoles indenting a muscle fiber. (d) Enlargement of area
circled in (c). Oxygen diffuses from the lumen of the tracheole (left) through the cuticle and the tracheolar cell to the
mitochondrion in the muscle fiber.
Fig. 17.2. Development of a tracheole (after Keister, 1948). (a) Tracheolar cell developing
from the tracheal epithelium. (b) Tracheolar cell with extensive cytoplasmic processes.
(c) Tracheole within tracheolar cell and becoming connected to existing trachea at a molt.
TRACHEAL SYSTEM 443
a) dorsal commissure
leg 1
prothorax
spiracle 1
spiracle 2
metathorax leg 3
imaginal disc of
hindwing
first abdominal
segment spiracle 3
b) heart
dorsal longitudinal
trunk
dorsal diaphragm
visceral trachea
gut
spiracle
lateral longitudinal
trunk
ventral diaphragm
nerve cord
ventral longitudinal
trunk
ventral commissure
Fig. 17.3. Tracheal system (from Snodgrass, 1935). (a) Tracheation of the thorax and first abdominal segment of a caterpillar,
dorsal view. (b) Diagrammatic cross-section of the abdomen of an orthopteran showing the principal tracheae and tracheal
trunks.
of the lumen connecting with the lumen of the trachea. which remains separate from the tufts of other spiracles. In
Wigglesworth calls these aeriferous tracheae and suggests the majority of insects, however, the tracheae from neigh-
that they functionally replace tracheoles as the primary boring spiracles join to form longitudinal trunks running
supply to the ovaries. the length of the body (Fig. 17.3). Usually there is a lateral
Review: Wigglesworth, 1983 trunk on either side of the body and these are often the
largest tracheae, while, in addition, dorsal and ventral lon-
17.1.3 Distribution of the tracheae within the insect gitudinal trunks may also be present. The longitudinal tra-
In those Collembola that have tracheae and in the cheae are connected to those of the other side of the body
Archaeognatha, the tracheae from each spiracle form a tuft by transverse commissures, while smaller branches extend
444 GASEOUS EXCHANGE
to the various tissues and, in turn, give rise to the trache- Each flight muscle has a primary supply consisting of a
oles. In general, the heart and dorsal muscles are supplied large tracheal trunk or airsac running alongside or through
by branches from the dorsal trunks, the alimentary canal, the muscle (Fig. 17.6). If a trachea forms the primary
gonads, legs and wings from the lateral trunks and the supply it widens to an airsac beyond the muscle. From the
central nervous system from the ventral trunks or trans- primary supply, small, regularly spaced tracheae arise at
verse commissures. right angles, running into the muscle. These form the sec-
The arrangement of tracheae tends to follow a similar ondary supply and they are often oval proximally, per-
pattern in each body segment, especially in larval forms mitting some degree of collapse, and taper regularly to the
and in the abdomen of adults. This basic arrangement is distal end. Finer branches pass in turn from these tracheae
modified, however, in the head, where there are no spira- into the muscles (Weis-Fogh, 1964a). In Odonata the ter-
cles, and in the thorax. The head is supplied with air from minal tracheolar branches run alongside and between the
spiracle 1 (often on the prothorax, see below) through two muscle fibers, but in close-packed and fibrillar flight
main tracheal branches on each side, a dorsal branch to the muscle they indent the fiber membrane and the finest tra-
antennae, eyes and brain and a ventral branch to the cheolar branches are closely associated with the mitochon-
mouthparts and their muscles. dria (Fig. 17.1c,d). Thus they are functionally within the
In actively flying insects, the oxygen demands of the muscle fiber, although anatomically they are still extracel-
flight muscles during flight greatly exceed those of all the lular. The tracheal supply to the flight muscles follows a
other tissues. It is essential that these demands should not similar pattern in all larger insects.
deprive other important tissues, such as the central nervous Major changes in tracheation occur only at a molt and,
system, of oxygen. In the desert locust, Schistocerca, this is in endopterygote insects, during the pupal period. For
achieved by effectively isolating the air supply to the thorax instance, the relative volume of tracheae in the ovaries of
from that to the rest of the body (Fig. 17.4). In addition, the Schistocerca increases 18 times at the penultimate molt and
two sides are isolated from each other. Even though the a further 16 times at the final molt. Between molts, the rel-
head is supplied from the first thoracic spiracle, its tracheal ative volume decreases because the ovary continues to
supply is also largely separated from the thoracic supply by grow; similar changes occur in the testes and male acces-
the small bore of some connecting tubes and the occlusion sory glands. Thus, as a tissue grows within a larval stage it
of others. This ensures a good and direct supply of air to becomes relatively less well supplied with oxygen. Possibly
the brain and major sense organs and, as the exhalent trunk shortage of oxygen stimulates mitosis in the tracheal cells,
from the head supplies the thoracic ganglia, these also have so that at the molt new tracheae are formed. New tracheae
a good air supply (Miller, 1960c). arise as columns of cells growing out from the existing tra-
To some extent, the distribution and abundance of tra- cheal epithelium (Fig. 17.7). A space develops between the
cheae and especially of tracheoles reflect the demands for cells and it becomes lined with cuticle and connects to the
oxygen by different tissues. Consequently, tracheoles are existing system at the next molt (Wigglesworth, 1954).
most abundant in areas of high metabolic activity, whether Small changes in the distribution of tracheoles may occur
this is associated with mechanical energy production, as in between molts. For instance, in the event of damage to the
flight muscles, or with chemical synthetic activity, as in epidermis, the epidermal cells produce cytoplasmic threads
pheromone glands. They are also very abundant in the which extend towards and eventually attach themselves to the
central nervous system, especially in the neuropil, perhaps nearest tracheole. These cytoplasmic threads, which may be
suggesting that synapses have a high demand for oxygen. 150 m long, are contractile and drag the tracheole to the
In the ganglia of the locust central nervous system, every region of oxygen-deficient tissue (Fig. 17.8). The normal dis-
point in the neuropil is within 10 m of a tracheole, but no tribution of tracheoles in the epidermis might arise in a
tracheal branching occurs in the outer parts of the gan- similar way (Wigglesworth, 1959). Changes in tracheole dis-
glion where the cell bodies are situated (Fig. 17.5) tribution occur in relation to flight muscle development in
(Burrows, 1980). The ovaries of several orders of insects pupae of cyclorrhaphan Diptera (see Fig. 15.25).
are supplied by aeriferous tracheae (see above), but the At least partly related to altered oxygen demands, the
rapidly developing terminal oocytes are individually sup- tracheal system varies with the state of development and
plied by many tracheoles (Wigglesworth, 1991). becomes more complex at each molt. This may involve
TRACHEAL SYSTEM 445
brain thoracic
airsac
subesophageal dorsal
ganglion orifice spiracle 1
degenerate ventral
trachea orifice
trachea to wing
muscles
mandibular
airsac
ventral longitudinal
degenerate trunk
tracheae
base of prothoracic
leg
b) anterior abdominal
thoracic airsac airsac
spiracle 1
cephalic
tracheae to gut
spiracle 2
ganglion 1
degenerate spiracle 5
leg 1 trachea
degenerate ventral longitudinal
trachea trunk
leg 2 leg 3
Fig. 17.4. Tracheal system of a locust (Schistocerca) (after Miller, 1960c). (a) Supply to the head from spiracle 1. Arrows
indicate the probable direction of airflow resulting from abdominal ventilatory movements. (b) Supply to the pterothorax.
Notice that the thoracic airsac is largely isolated from other parts of the tracheal system by narrow or degenerate tracheae.
446 GASEOUS EXCHANGE
interganglionic
connective
openings of
17.1.4 Molting the tracheal system
b)
secondary The cuticular lining of the tracheae is cast at each molt,
supply shunt
and a new, larger intima formed in its place. The longitudi-
nal trunks break at predetermined points, the nodes,
between adjacent spiracles and the old lining is drawn out
primary
supply secondary through the spiracles and shed with the rest of the exuviae.
supply
Where the number of functional spiracles is reduced, the
muscle ‘non-functional’ spiracles persist and facilitate the shed-
ding of the tracheal intima so that this can occur even in
Fig. 17.6. Tracheal supply to the flight muscles. Arrows indicate
the inward flow of air (after Weis-Fogh, 1964a). (a) Primary
apneustic insects. The ‘non-functional’ spiracles may be
supply is a trachea ventilated by an airsac outside the muscle. (b) visible as faint scars on the cuticle. From each scar, a strand
Primary supply is an airsac directly associated with the muscle. of cuticle (formed from a collapsed trachea) connects with
the longitudinal trachea and, at each molt, a tube of new
cuticle is laid down round it. The old intima is withdrawn
through the tube which subsequently closes and forms the
cuticular strand connecting the new intima with the outer
TRACHEAL SYSTEM 447
tracheole
cuticles before each ecdysis. The liquid is replaced by gas in there is never more than one pair of spiracles on a segment,
a process known as pneumatization. In terrestrial insects, usually on the pleuron. Often, each spiracle is contained in
gas may enter via the spiracles, but pneumatization occurs a small, distinct sclerite, the peritreme.
in aquatic insects, and in many terrestrial species without
access to air. Gas usually appears first in a main tracheal 17.2.1 Number and distribution
trunk and then spreads rapidly through the system which The largest number of spiracles found in insects is ten
becomes completely gas-filled in 10–30 minutes. The gas is pairs, two thoracic and eight abdominal, and the respira-
probably forced out of solution in the liquid by physical tory system can be classified on the basis of the number
forces resulting from the active resorption of liquid from and distribution of the functional spiracles (Keilin, 1944).
the tracheae together with the change in the surface prop- In numerous insects, the first spiracle is on the prothorax,
erties from hydrophile to hydrofuge which occurs when the but is mesothoracic in origin (Hinton, 1966). Spiracles are
cuticle is tanned. These forces lead to the rupture of the never present on the head.
liquid column and the appearance of gas in its place.
In many insects, some liquid normally remains in the Polypneustic – at least 8 functional spiracles on each side
endings of the tracheoles. During periods of high energy Holopneustic – 10 spiracles: 1 mesothoracic, 1 meta-
consumption the liquid is withdrawn from the system and thoracic, 8 abdominal – as in dragonflies, grasshoppers,
air is drawn further into the tracheoles. At other times, the cockroaches, fleas and some hymenopteran and dipte-
liquid is secreted again and the air retreats. The level of ran larvae such as the larvae of Apis and Bibio
liquid in the tracheoles represents the balance between the Peripneustic – 9 spiracles: 1 mesothoracic, 8 abdominal –
forces of capillarity and forces resulting mainly from imbibi- as in caterpillars and many other endopterygote larvae
tion due to colloidal substances in the cytoplasm of the tra- Hemipneustic – 8 spiracles: 1 mesothoracic, 7 abdominal –
cheolar cell. These, in turn, are influenced by changes in the as in mycetophilid larvae
osmotic pressure of the tissues. When the metabolic rate is Oligopneustic – 1 or 2 functional spiracles on each side
high, osmotic pressure rises and fluid is withdrawn from the Amphipneustic – 2 spiracles: 1 mesothoracic, 1 posterior
tracheoles; when it is low, osmotic pressure falls and capillar- abdominal – as in many larval Diptera, especially
ity draws fluid into the tracheoles. The initial withdrawal of amongst the Cyclorrhapha
liquid from the tracheae after molting may similarly result
Propneustic – 1 spiracle: 1 mesothoracic – as in mosquito
from metabolic changes (Wigglesworth, 1983).
pupae
Metapneustic – 1 spiracle: 1 posterior abdominal – as in
17.2 SPIRACLES mosquito and some aquatic beetle larvae
The spiracles are the external openings of the tracheal Apneustic – no functional spiracles – as in many aquatic
system. They are lateral in position, and in the Insecta, larvae. Apneustic does not imply that the insect has no
SPIRACLES 449
closer
muscle
cuticular
sclerotized process
membrane pad
c)
anterior posterior
valve valve
mesepimeron metepisternum
closer
ligament muscle
atrium
process from ventral
sclerotized rod orifice closer
muscle
closer opener
muscle muscle
opener
inflexion of muscle
cuticle
17.2.3 Control of spiracle opening contraction of the closer muscle, while opening commonly
The spiracles are normally open for the shortest time nec- results from the elasticity of the surrounding cuticle when
essary for efficient respiration presumably to keep water the closer muscle is relaxed. The muscle is controlled by
loss from the tracheal system to a minimum (but see the central nervous system, but may also respond to local
below). Spiracle closure results from the sustained chemical stimuli.
SPIRACLES 451
a) sclerotized
band
closer c) closer
muscle muscle
rigid bar
atrium movable
lever
elastic flexible
opening rod
ligament
trachea
hinge
spiracle
b) opening atrium
d)
cuticle trachea
flexible
rod
rigid bar
epidermis
closer
movable muscle
trachea lever
Fig. 17.13. Closing mechanisms internal to the spiracle. (a),(b) Abdominal spiracle of a caterpillar seen from inside (a) and in
horizontal section (b) (from Imms, 1957). (c),(d) Constricting mechanism on a trachea of a flea seen in horizontal section (c)
and from above (d) (after Wigglesworth, 1965).
The motor neurons to the spiracle muscles in each Both these conditions tend to arise while the spiracles are
segment arise in the ganglion of the same segment or that closed as carbon dioxide is produced and oxygen is utilized
immediately in front. The closer muscles in dragonflies, in respiration. Both conditions lead to a reduction in
Periplaneta and Schistocerca are innervated by two motor action potential frequency and so to spiracle opening. In
neurons whose axons pass along the median nerve and ‘two muscle’ spiracles the action potential frequency to the
then bifurcate, sending a branch to either side, so that the opener muscle is increased by high carbon dioxide levels
two spiracles receive the same pattern of motor impulses and hypoxia.
(see Fig. 17.21). Closer muscles may also be innervated by The frequency of motor impulses to the closer muscle is
an inhibitory axon. The opener muscle, when it is present, also affected by the water balance of the insect, possibly
is innervated from one or two neurons whose cell bodies acting through the concentration of a particular ion. If the
are usually lateral in the ganglion and the spiracles of the insect is desiccated, action potential frequency rises and the
two sides are independently innervated. In Blaberus and spiracles remain closed longer; with excess hydration, the
related cockroaches, a common inhibitory neuron inner- converse is true and so the rate of water loss is increased.
vates a number of abdominal spiracle opener muscles. Carbon dioxide also acts directly on the closer muscle
The closer muscle is caused to contract by the activity of ‘one muscle’ spiracles, interfering with neuromuscular
of its motor neurons, but the frequency of action poten- transmission so that the junction potential falls, muscle
tials, determining the degree of contraction, may be tension is reduced and the spiracle opens (Hoyle, 1960).
altered by various factors acting on the central nervous The threshold of the peripheral response to carbon
system. Of particular importance are a high level of carbon dioxide is set by the frequency of motor impulses from the
dioxide and a low level of oxygen (hypoxia) in the tissues. central nervous system. The lower the impulse frequency,
452 GASEOUS EXCHANGE
the lower the threshold to carbon dioxide. Carbon dioxide mitochondria in order to play a part in oxidative processes.
has some other, internal, effect on the muscle, not con- There are thus two distinct phases in the transport of
nected with neuromuscular transmission, and this also gases, one through the tracheal system, known as air-tube
results in a reduction in tension. ‘Two muscle’ spiracles do diffusion, and one through the tissues in solution in the
not respond to peripheral stimulation by carbon dioxide cytoplasm, known as tissue diffusion (Weis-Fogh, 1964b).
and are controlled entirely by the output from the central
nervous system (Miller, 1960b). 17.4.1 Diffusion
Hemolymph potassium has a direct effect on some The rate of diffusion of a gas depends on a number of
spiracle muscles. In the case of spiracle 2 of Schistocerca, a factors. It is inversely proportional to the square root of the
‘one muscle’ spiracle, concentrations of potassium above molecular weight of the gas, so that in air, oxygen, with a
30 mM cause the closer muscle to contract even when it is molecular weight of 32, diffuses 1.2 times faster than
isolated from the nervous system (Hoyle, 1961). Normally carbon dioxide, molecular weight 44. Diffusion also
the concentration in the blood is not as high as this, but it depends on the differences in concentration (the
may be exceeded as a result of desiccation and also at the concentration gradient) of the gas at the two ends of the
molt. Consequently, under these circumstances, the spira- system and, in the absence of a difference in concentration,
cles remain closed for most of the time, opening only when there is no net movement of gas. The change in concentra-
the concentration of carbon dioxide in the tissues is high. tion, or partial pressure (p), with distance (x) is expressed
This is presumed to restrict water loss. Such sustained as ␦p/␦x. Finally, the permeability of the substrate, in this
muscular contraction due to high concentrations of potas- case air or the tissues, through which the gas is diffusing
sium does not occur in other muscles. affects the rate of diffusion. This factor is expressed in
Review: Kaars, 1981 terms of the permeability constant, P, which is the flow of
a substance through unit area per unit time when the
concentration gradient is unity. Hence, the volume (J) of a
17.3 CUTANEOUS RESPIRATION
given gas transported by diffusion at normal temperature
Some gaseous exchange takes place through the cuticle of and pressure (NTP) can be represented by the equation
most insects, but does not usually amount to more than a
J ⫽⫺P␦p/␦x (Weis-Fogh, 1964b).
small percentage of the total gaseous movement. On the
other hand, Protura and most Collembola have no tracheal The permeability constant for different substrates
system and must depend on cutaneous respiration together varies widely. That for oxygen in air at 20 °C is approxi-
with transport by the hemolymph from the body surface to mately 0.11 ml min⫺1 cm⫺2 kPa⫺1 cm⫺1 whereas in
the tissues. Cutaneous respiration is also important in many water P ⫽ 0.34 ⫻ 10⫺6 and in frog muscle
endoparasitic and aquatic insects where it is coupled with an 0.14 ⫻ 10⫺6 ml min⫺1 cm⫺2 kPa⫺1 cm⫺1. Hence
apneustic tracheal system. Cutaneous respiration without oxygen in air diffuses more than 100 000 times faster
an associated apneustic tracheal system can only suffice for than in water or the tissues, so that although, in the
very small insects with a high surface/volume ratio. insect, the path of oxygen through the tracheal system is
The impermeability of most insect cuticles to oxygen very much longer than its path through the tissue, it will
arises from the epicuticle, but not from the wax layer probably take longer for the gas to diffuse from the
which renders the cuticle impermeable to water (Buck, tracheole endings to the mitochondria, than from the
1962). The permeability to carbon dioxide may be rather spiracles to the tracheole endings.
greater and the loss of this gas through the intersegmental Thus, the length of the tissue diffusion path is likely to
membranes may be appreciable. be a factor limiting the size of tissues and, in particular, of
flight muscles with a high requirement for oxygen. With a
partial pressure difference between the tracheole and the
17.4 GASEOUS EXCHANGE IN TERRESTRIAL
mitochondrion of 5 kPa, a tracheole 1 m in diameter
INSECTS
would serve a muscle 7–15 m in diameter if the oxygen
Oxygen passes through the tracheal system from the uptake of the muscle was 1.5–3.0 ml g⫺1 min⫺1, a level of
spiracles to the tissues and ultimately must reach the uptake achieved in flight muscle. Hence a muscle fiber in
GASEOUS EXCHANGE IN TERRESTRIAL INSECTS 453
which the tracheoles are restricted to the outside of the follows that the tracheoles are generally a more important
fibers cannot exceed about 20 m in diameter. The fibers of site of gaseous exchange with the tissues than are the more
the flight muscles of dragonflies are of this type and are proximal tracheae (assuming that the permeability of their
approaching their theoretical maximum size. On the other cuticular linings is similar).
hand, if the tracheoles indent the muscle so as to become It has generally been supposed that gaseous exchange
functionally internal, as they do in flight muscles of most in small or quiescent insects depended entirely on
insects, the muscle fibers can become much larger. In diffusion. However, more critical theoretical analysis of the
Musca (Diptera), for instance, the indenting tracheoles are system has led this belief to be questioned (Kestler, 1985).
only separated by distances of 3–5 m and lie very close to At the same time, experimental methods have demon-
the mitochondria so that, although individual fibers may be strated that in most resting adult insects, including some
over one millimeter in diameter, they are well within the small ants and even phorid flies weighing less than 1 mg,
size limits imposed by tissue diffusion (Weis-Fogh, 1964b). gaseous exchange depends on convective movements of
Due to its greater solubility, the permeability constant of gas into and from the tracheal system in addition to
carbon dioxide in the tissues is 36 times greater than that for diffusion (Miller, 1981b). The extent to which diffusion
oxygen, so that despite its higher molecular weight, carbon alone is important is thus an open question, although some
dioxide travels more quickly than oxygen through the worker ants appear not to engage in active ventilation.
tissues for the same difference in partial pressure. Hence a Presumably in aquatic insects with a closed respiratory
system capable of bringing an adequate supply of oxygen to system, diffusion normally serves to transport oxygen
the tissues will also suffice to take the carbon dioxide away. from the gills to the tissues.
As carbon dioxide is more soluble, it is present in Review: Kestler, 1985 – theoretical considerations
higher concentrations in the tissues than oxygen. Thus
some carbon dioxide, instead of passing directly into the 17.4.2 Ventilation
tracheal system, may be temporarily retained in the hemo- Ventilation of the tracheal system involves the convective
lymph before diffusing into the tracheae near the spiracles movements of gases. These movements are produced pri-
or passing out directly through the integument. marily by changes in the volume of the tracheal system
The exchange of gases between the tracheal system and although reduced pressure within the tracheae due to the
the tissues is partly limited by the walls of the tracheae and utilization of oxygen may also be important in some cases.
tracheoles. The whole system may be permeable, with no This is known as passive suction ventilation.
marked difference between tracheoles and tracheae, but it Most tracheae are circular in cross-section and resist
is generally believed that the lining of the tracheoles is any change in form because of their taenidia, but some,
more permeable, especially in flight muscles such as the longitudinal trunks of larval Dytiscus
(Wigglesworth, 1983, but see Wigglesworth, 1990a). In (Coleoptera) are oval in cross-section and are subject to
any case, as the tracheoles are more closely associated with compression. The compression of a trachea forces air out
the tissues they will, in general, be more important than of the tracheal system, while its subsequent expansion
the tracheae in the transfer of oxygen to the tissues. sucks air in again. But changes in shape of the trachea, if
The rate of gaseous exchange also varies with the they occur at all, only produce small volume changes.
surface area through which the gases are diffusing. In some Much larger changes, and hence better gaseous exchange,
insects, the summed cross-sectional area of the tracheal are produced by the alternating collapse and expansion of
system at different distances from the spiracles is believed airsacs. Compression of the system, causing expiration,
to remain constant. Distally this area is made up of many results indirectly as a result of hemolymph pressure. This
small tubes (tracheoles), proximally (near the spiracle) of a is achieved in two ways: by reduction in the body volume,
few large ones (tracheae), so that the summed circumfer- usually of the abdomen, and by displacement of hemo-
ence or wall area/unit length is much greater distally than lymph from different parts of the body while the total body
proximally. Although, in Bombyx larva, the summed cross- volume remains constant. Expansion of the airsacs and
sectional area of the tracheoles is less than that of the tra- inspiration result from the reduction of pressure due to
cheae, the wall area/unit length of the tracheoles is the muscular or elastic expansion of the abdomen or the
nevertheless greater (Buck, 1962). As this is so, it again movement of hemolymph to another part of the body.
454 GASEOUS EXCHANGE
a) b)
airsac
heart
c)
CO2 emission (µl.min -1)
4
heartbeat forward back forward back
0 20 40 60
time (s)
Fig. 17.15. Discontinuous gas exchange associated with reversals of the heartbeat in a fly (Calliphora). The tracheal system
is represented diagrammatically (after Wasserthal, 1996). (a) Forward beating of the heart draws hemolymph from the
abdomen and pushes it into the thorax and head. This expands abdominal airsacs and compresses those in the head and
thorax so that air is drawn in through abdominal spiracles and forced out through thoracic spiracles. (b) Backwards beating
of the heart draws hemolymph from the head and thorax and pushes it into the abdomen. This compresses abdominal airsacs
and expands those in the head and thorax so that air is drawn in through thoracic spiracles and forced out through abdominal
spiracles. (c) Carbon dioxide is emitted when the heart is beating in either direction, but more is forced out from the abdomen
than the thorax due to the greater volume of airsacs in the former.
reduced and the compression phase eliminated (Fig. about 20% of the volume at each stroke. Neck and protho-
17.16b). The net time for which the spiracles are open racic ventilation provide a further 50 ml air g⫺1 h⫺1. In
increases as a result (Miller, 1960b). Dytiscus, 60% of the air is renewed with each compression
After periods of activity, abdominal ventilation is and expansion.
supplemented by other types of ventilation and in Reviews: Miller, 1981b; Wasserthal, 1996
Schistocerca these involve protraction and retraction of the
head on the prothorax (neck ventilation), and movement 17.4.3 Discontinuous gas exchange
of the prothorax on the mesothorax (prothoracic ventila- Although ventilation is often continuous, there may be
tion) (Miller, 1960a). These movements primarily venti- extended periods during which all the spiracles are closed.
late the head. The normal level of abdominal ventilation in The movement of oxygen into the tracheae and carbon
Schistocerca pumps about 40 ml air g⫺1 h⫺1 through the dioxide emission then occur in discrete bursts when the spir-
body, about 5% of the air being exchanged at each move- acles open; relatively little gas exchange occurs while they
ment, but this can be raised to 150 ml, with an exchange of are closed. This phenomenon is known as discontinuous gas
456 GASEOUS EXCHANGE
b) hyperventilation
open
spiracle 10
(expiration)
closed
open
spiracle 2
(inspiration)
closed
5 seconds
exchange or discontinuous ventilation. It is common in adult ling the activities of the spiracle and movements of gases
insects when they are inactive at moderate temperatures, are not necessarily the same in all cases. In many instances,
that is, when their metabolic rates are low. The pupae of carbon dioxide release is associated with reversal of the
many insects also exhibit discontinuous gas exchange. heartbeat. This occurs even in pupal Lepidoptera where
The periodicity of ventilatory bouts varies from insect the interval between bursts is several hours, but in this
to insect and with environmental conditions. In diapausing case carbon dioxide release does not occur with every
pupae of the moth, Hyalophora, the interval between spir- reversal of the heartbeat (Wasserthal, 1996).
acle openings is as long as eight hours. In some resting The process is most fully understood in pupal
grasshoppers at 15 °C, carbon dioxide is released about Lepidoptera. At the end of a burst (spiracles open) in
once per hour, but at 30 °C the period of spiracle closure is Hyalophora pupa, oxygen comprises about 18% of the gas
reduced to about five minutes (Quinlan & Hadley, 1993). in the tracheae. The spiracles close tightly and, as the
In the beetle, Psammodes, each cycle lasts about 15 minutes oxygen is used up, the pressure in the tracheae falls. At the
(Fig. 17.17), while in some ants and the honeybee it is less same time there is only a small increase in the proportion
than five minutes (Fig. 17.18) (Lighton, 1988; Lighton & of carbon dioxide present, most of it being dissolved in the
Berrigan, 1995; Wasserthal, 1996). hemolymph. The low oxygen content of the tracheal air
During the closed phase, relatively little gas exchange and tissues is monitored by receptors associated with the
takes place (Fig. 17.17). As carbon dioxide is produced it is central nervous system and hypoxia reduces activity in the
presumed to be dissolved in the hemolymph. When the spir- motor neurons to the closer muscles so that the spiracles
acles open, oxygen rushes into the system and carbon dioxide open slightly. Because of the low pressure in the tracheal
and water vapor diffuse out. In some insects, such as system, air rushes in. The bulk influx of air limits the
Psammodes, ventilatory movements of the abdomen are made outward diffusion of water vapor and of carbon dioxide,
during this period so that gases are actively pumped in and which therefore continues to accumulate in the tracheae
out of the system until the spiracles close again (Fig. 17.17b). and the tissues. Diffusion probably also contributes to the
Between the periods of complete closure and com- inward movement of oxygen because of the low partial
plete opening, some insects exhibit a period in which the pressure of oxygen in the tracheae. The influx of air tem-
spiracles repeatedly open slightly and close again, a porarily increases the amount of oxygen present, so that
movement called fluttering. During this period, oxygen the spiracles close again. The repeated lowering and
enters the system, but relatively little carbon dioxide raising of the oxygen level leads to the fluttering movement
escapes from it (Fig. 17.17c,d). The mechanisms control- of the spiracle valves. Slowly, however, carbon dioxide
GASEOUS EXCHANGE IN TERRESTRIAL INSECTS 457
a) spiracle activity
open
flutter
closed
b) abdominal contractions
rate 10
(number.min -1)
0
c) oxygen uptake
0.4
oxygen uptake
(ml.g -1.h-1)
d) CO 2 emission
0.4 accumulates in the hemolymph. Ultimately, it reaches a
CO2 emission
loss through accounts for the inward movement of oxygen as the partial
cuticle
pressure in the system is continuously falling as it is used
in oxidative processes (Lighton & Garrigan, 1995).
As a consequence of discontinuous gas exchange, the
0 5 10 15 spiracles are closed for most of the time. As water loss
time (minutes) through the spiracles is greatly enhanced during periods of
Fig. 17.17. Discontinuous gas exchange in a beetle (Psammodes). spiracle opening, it has been assumed that the limitation of
Changes occurring in a single bout of ventilation (after Lighton, water loss is the evolutionary raison d’être for discontinuous
1988). (a) Activity of the spiracles. During the flutter phase, gas exchange. However, as the amount of water lost through
they open slightly for brief periods and then close again. (b) the spiracles is usually very small relative to that lost via the
Abdominal ventilation coincides with the open phase of the cuticle, the general application of this argument has been
spiracles. (c) Oxygen uptake. Some occurs during flutter, but the questioned (Hadley, 1994; Lighton, 1994; Lighton &
rate is greatly increased when the spiracles open fully. (d) Carbon Berrigan, 1995) although it may be valid for pupal stages
dioxide emission is largely confined to the open phase of the
and in insects with relatively high rates of spiracular water
spiracles. Very little occurs during spiracular flutter. (e) Water
loss (Lighton et al., 1993b; Williams, Rose & Bradley, 1997).
loss increases when the spiracles open.
Reviews: Hadley, 1994; Lighton, 1994, 1996; Sláma, 1988
458 GASEOUS EXCHANGE
I E I E I E I E I E I I E I E I E I E I E I
open
spiracle 1
(inspiration)
closed
open
spiracle 2
(inspiration and
expiration in flight)
closed
open
spiracle 10
(expiration)
closed
compressed
ventilation
expanded
5 seconds
Fig. 17.20. Spiracle activity and abdominal ventilation during flight of Schistocerca. I, inspiration; E, expiration (after Miller,
1960c).
pterothoracic ventilation produces an airflow of about These spiracles supply the flight muscles, and, since the
350 ml air g⫺1 h⫺1, which is adequate for the needs of the tracheal system of these muscles is largely isolated and the
flight muscles. spiracles remain open all the time, there is a tidal flow of air
Thoracic pumping is also important in flight in in and out of them (Miller, 1960c).
Odonata and probably in Lepidoptera and Coleoptera. In
Hymenoptera and Diptera, changes in the thoracic volume 17.4.5 Control of ventilation
during flight are not very large and abdominal pumping is As in the control of spiracles, ventilatory movements are
of greater importance in maintaining the air supply to the initiated by the accumulation of carbon dioxide and, to a
flight muscles (Weis-Fogh, 1964a). In a large cerambycid lesser extent, the lack of oxygen in the tracheal system
beetle, Petrognatha, there is evidence that a stream of air, (Gulinson & Harrison, 1996), acting directly on centers in
resulting from the forward movement of the insect in the ganglia of the central nervous system. Each abdominal
flight, flows in through the forwardly directed second spir- ganglion produces rhythmical sequences of activity con-
acles into large tracheae running directly to the third spira- trolling the movements. In Schistocerca and Periplaneta,
cles. This stream of air ventilates the primary supply to the the metathoracic ganglion acts as a pacemaker and over-
flight muscles while the secondary supply is probably ven- rides the rhythms of the other ganglia (Lewis, Miller &
tilated by muscular compression (Miller, 1966a). Mills, 1973).
When Schistocerca starts to fly, the pattern of spiracle In normal ventilation by Schistocerca, involving only
opening also alters (Fig. 17.20). At first, spiracles 1 and 4 to dorso-ventral movements of abdominal sclerites, expira-
10 close, but then they open and close rhythmically in syn- tion is produced by tergosternal muscles innervated by
chrony with abdominal ventilation so that there is a flow of motor neurons from the ganglion of the corresponding
air via the head to the rest of the central nervous system. segment. Inspiration is produced by muscles inserted low
Increased abdominal ventilation may also improve the on the tergum and innervated by axons in branches from
blood circulation and hence the fuel supply to the flight the median ventral nerve. The perikarya of these motor
muscles. Spiracles 2 and 3 remain wide open throughout neurons are in the ganglion of the preceding segment, so
flight and although they show some incipient closures after that the alternation of inspiratory and expiratory move-
a time these do not affect the airflow through the spiracles. ments is controlled from different ganglia (Fig. 17.21a).
460 GASEOUS EXCHANGE
dorso-ventral
muscles longitudinal
a) muscles
inspiratory expiratory
inspiratory
VENTILATION expiratory
4
5
ganglion 5 ganglion 6
median ventral
nerve connective
perikarya of
motor neurons
SPIRACLES
closer opener
muscle muscle
b)
metathoracic abdominal
ganglion ganglion
2
inputs from central to posterior
anterior pattern ganglia
centers generator
2
4 4 4 5 5
interneuron
6
motor neuron
excitatory synapse
inhibitory synapse
to expiratory to inspiratory
muscles muscles
Fig. 17.21. Control of spiracles and ventilatory movements in a locust (Schistocerca). (a) Innervation of ventilatory muscles
(top) and spiracular muscles (bottom). The cell bodies of motor neurons controlling the muscles of one segment are not
confined to the ganglion of that segment; some are in the ganglion of the next anterior segment. The axons in the median
nerve divide (arrow) so that homologous muscles on the two sides are innervated by the same neurons. Notice that the
ventilatory muscles and spiracular muscles are not controlled by the same neurons. Numbers adjacent to cell bodies in
ganglion 5 relate to the cells shown in (b) (based on Lewis, Miller & Mills, 1973). (b) Diagram showing the control of
ventilatory muscles. The interneurons (2) are driven by a central pattern generator and extend to all the abdominal ganglia.
Motor neurons are numbered to correspond with the same numbers in (a). See text for further explanation (based on Lewis,
Miller & Mills, 1973; Pearson, 1980).
GASEOUS EXCHANGE IN AQUATIC INSECTS 461
Coordination is achieved by a coordinating interneuron, that oxygen can readily pass from the water into the
one in each ventral connective (cell 2 in Fig. 17.21b), tracheae.
which originates in the metathoracic ganglion and extends
to the last abdominal ganglion. These interneurons are 17.5.1 Aquatic insects obtaining oxygen from the air
driven by a central pattern generator, probably in the Most aquatic forms obtaining air from above the water
metathoracic ganglion, whose activity is regulated by surface must make periodic visits to the surface, but a few
inputs from the head and other parts of the body. Action have semipermanent connections with the air that enable
potentials in the interneuron have an excitatory effect on a them to remain submerged indefinitely. The larva of the
local interneuron (cell 3) and probably have a weak direct hover fly, Eristalis (Diptera), has a telescopic terminal
inhibitory effect on the inspiratory motor neurons (cell 5 in siphon which can extend to a length of six centimeters or
Fig. 17.21b). The local interneuron excites the expiratory more in a larva only one centimeter long. By means of the
motor neurons (cell 4) and strongly inhibits the inspiratory siphon the larva can reach the water surface with its poste-
motor neurons (cell 5). Inspiration occurs when the inter- rior spiracles, while the body remains on the bottom mud
segmental interneurons are silent and the inspiratory (Fig. 17.22).
motor neurons become spontaneously active, at the same Some other species obtain oxygen by thrusting their
time inhibiting the expiratory motor neurons via another spiracles into the aerenchyma of aquatic plants. This habit
local interneuron (cell 6) (Lewis et al., 1973; Pearson, occurs in larval Donacia (Coleoptera) and Chrysogaster
1980). (Diptera), and larvae and pupae of Notiphila (Diptera) and
The rate of ventilation is altered by reducing the inter- the mosquito Mansonia. With the exception of Mansonia, all
val between inspiratory bursts and is affected by sensory of these species live in mud containing very little free
input from various sources. Centers sensitive to carbon oxygen (Varley, 1937). The functional spiracles are at the tip
dioxide are present in the head and thorax of Schistocerca of a sharp-pointed post-abdominal siphon in larval forms
and these modify the activity of the pacemaker, while the (Fig. 17.23) and on the anterior thoracic horns of the pupae.
output is also modified by high temperature and nervous For most aquatic insects obtaining their oxygen from the
excitation generally. Proprioceptors may play some part air, however, periodic visits to the surface of the water are
in the maintenance of the frequency of ventilation necessary to renew the gases in the tracheal system.
(Miller, 1960a; Farley and Case, 1968). The coordination Problems facing all insects which come to the surface are
of the spiracles with the ventilatory movements is those of breaking the surface film and of preventing the
brought about by motor patterns derived from the venti- entry of water into the spiracles when they submerge. The
latory centers. ease with which this is accomplished depends on the surface
Review: Miller, 1966a properties of the cuticle and, in particular, on its resistance
to wetting. When a liquid rests on a solid or a solid dips into
a liquid, the liquid/air interface meets the solid/air inter-
17.5 GASEOUS EXCHANGE IN AQUATIC
face at a definite angle that is constant for the substances
INSECTS
concerned. This angle, measured in the liquid, is known as
Aquatic insects obtain oxygen directly from the air or the contact angle (Fig. 17.24). A high contact angle indicates
from that dissolved in the water. The former necessitates that the surface of the solid is only wetted with difficulty and
some semi-permanent connection with the surface or fre- such surfaces are said to be hydrofuge. Under these condi-
quent visits to the surface. Insects that obtain oxygen from tions, the cohesion of the liquid is greater than its adhesion
water nearly always retain a tracheal system so that the to the solid, and so, when an insect whose surface properties
oxygen must come out of solution into the gaseous phase. are such that the contact angle is high comes to the
This is important because the rate of diffusion in the gas air/water interface, the water falls away leaving the body dry
phase is very much greater than in solution in the hemo- (Holdgate, 1955). The whole surface of the cuticle may
lymph. Gaseous exchange with water takes place through possess hydrofuge properties, so that it is not readily wetted
thin-walled gills well supplied with tracheae, but in other at all, or these properties may be restricted to the region
cases a thin, permanent film of air is present on the around the spiracles. In dipterous larvae, for example,
outside of the body. The spiracles open into this film so perispiracular glands produce an oily secretion in the
462 GASEOUS EXCHANGE
air
air
solid solid
respiratory siphon
water
contact water contact
angle angle
substratum
Fig. 17.22. Semi-permanent connection with the water surface. SUBMERGED AT SURFACE
The larva (rat-tailed maggot) of the hover fly, Eristalis, with its
respiratory siphon partly extended (after Imms, 1947). hairs close over hairs separated by
spiracle preventing tension forces,
entry of water spiracle exposed
a) saw
teeth
Fig. 17.25. Diagrams showing the movements of hydrofuge hairs
surrounding a spiracle when an insect is submerged and at the
surface. The movement of the hairs is entirely passive, depending
on physical forces acting between the hairs and the water
b) (modified after Wigglesworth, 1965).
respiratory
spiracle siphon
immediate neighborhood of the spiracle. Often hydrofuge
properties round the spiracle are associated with hairs, as in
Notonecta (Heteroptera), or valves, as in mosquito larvae,
which close when the insect dives, but open at the surface
(Fig. 17.25), being spread out by surface tension.
In many of these insects, only the posterior spiracles
anal segment
are functional and they are often carried on the end of a
siphon extending from the posterior body, as in larval
trachea Ephydridae and Culicidae. In these insects, only the tip of
the siphon breaks the surface film. In water scorpions
Fig. 17.23. Semi-permanent connection with the aerenchyma of
a plant. The respiratory siphon of a mosquito larva (Mansonia)
(Hemiptera, Nepidae), the spiracles are at the base of an
which connects with the aerenchyma of aquatic plants (after air-filled tube.
Keilin, 1944). (a) Lateral view showing saw which cuts into the An increase in the number of functional spiracles often
plant tissue and recurved teeth which hold the siphon in place. occurs in the last stage larva since this stage is commonly
(b) Longitudinal section showing a terminal spiracle and a less strictly aquatic than earlier stages, leaving the water in
trachea. order to pupate or, in hemimetabolous insects, to facilitate
GASEOUS EXCHANGE IN AQUATIC INSECTS 463
in air
oxygen - 21%
nitrogen - 78%
carbon dioxide - 0.03% insect dives insect uses oxygen equilibrium
from bubble restored
Fig. 17.26. Diagram of an air bubble acting as a physical gill. As the insect dives, the gases in the bubble are in equilibrium
with those dissolved in the water. As the insect uses oxygen, the equilibrium is perturbed. It is restored by the inward
movement of oxygen and the outward movement of nitrogen. This is a continuous process; it is shown as two separate steps
for clarity. Note that carbon dioxide produced by the insect is immediately dissolved in the water. Oxygen comes out of
solution faster than nitrogen goes in. The bubble shrinks continuously as nitrogen goes into solution.
adult emergence. The number of functional spiracles soon as the insect stops swimming or releases its hold on
never decreases from one instar to the next (Hinton, 1947). the vegetation, it floats to the surface. The position of the
store is such that the insect breaks the surface suitably ori-
17.5.1.1 Gas exchange via air bubbles ented to renew the air. Dytiscus, for instance, comes to the
Some insects, such as mosquito larvae, can remain sub- surface tail first and renews the subelytral air from the pos-
merged only as long as the supply of oxygen in the tracheae terior end of the elytra.
lasts, but others have an extra-tracheal air store, carrying a
bubble of air down into the water when they dive. The Physical gills An air bubble provides an insect with more
spiracles open into this bubble, so that it provides a store of oxygen than that available at the time of the dive because it
air additional to that contained in the tracheal system, also acts as a temporary gill. When an insect dives, the gases
enabling the insects to remain submerged for longer in its air store are in equilibrium with the gases dissolved in
periods than would be possible without it. the water, assuming that this is saturated with air. Normally,
The position of the store is characteristic for each at the dive, the bubble would contain approximately 21%
species. In Dytiscus, it is beneath the elytra, and experi- oxygen and 79% nitrogen, while the water, because of the
mental removal of the hind wings increases the space differing solubilities of the gases, will contain 33% oxygen,
beneath the elytra and enables the insect to remain 64% nitrogen and 3% carbon dioxide (Fig. 17.26). Carbon
submerged for longer periods. In Notonecta, air is held by dioxide is very soluble, so there is never very much in the
long hydrofuge hairs on the ventral surface as well as in a bubble. Within a short period of diving, the proportion of
store under the wings and in a thin film held by small bris- oxygen in the bubble is reduced, as the oxygen is utilized by
tles over the dorsal surface of the fore wing. The related the insect, and there is a corresponding increase in the pro-
Anisops (Heteroptera) has ventral and subelytral stores portion, and hence partial pressure, of nitrogen. As a result,
supplemented by oxygen loosely associated with hemo- the gases in the bubble and those in solution immediately
globin in large hemoglobin cells just inside the abdominal surrounding it are no longer in equilibrium and movements
spiracles (section 17.9). of gases will occur tending to restore equilibrium. Oxygen
An air store also gives the insect buoyancy, so that as tends to pass into the bubble from the surrounding
464 GASEOUS EXCHANGE
17.5.2 Insects obtaining oxygen from the water 17.5.2.1 Tracheal gills
In all insects living in water, some inward diffusion of oxygen In some insects, such as Simulium larvae, there is a network
from the water takes place through the cuticle and in many of tracheoles just beneath the general body cuticle, but
larval forms gaseous exchange takes place solely in this way. often there are leaf-like extensions of the body forming
GASEOUS EXCHANGE IN AQUATIC INSECTS 465
pre-branchial diaphragm
a) valve 5 4
6
7
vestibule 8
9
10
branchial chamber
anus
dilator
muscles
dilator sub-intestinal
muscle muscle
b)
dorsal
trachea c) longitudinal
muscle
lumen of
branchial gut
chamber
gill
lamella
chloride dorso-ventral
cells muscle sub-intestinal
muscle
wall of ventral
branchial trachea
chamber
d) water in
rectum
cuticle
trachea
epidermis
basal lamina
hemolymph nucleus
Fig. 17.29. Tracheal gills in the rectum of a dragonfly larva (after Mill & Pickard, 1972; Tillyard, 1917). (a) Longitudinal
section through the abdomen. Numbers indicate abdominal segments. (b) Transverse section through the branchial chamber
(c) Transverse section through abdominal segment 6 showing the subintestinal muscle. (d) Detail of gill epithelium showing
the tracheae close beneath the cuticle (after Schmitz & Komnich, 1976).
close together, at about 2 500 000 mm⫺2, and are able to pores. These canals are lined with hairs so that the entry
withstand a pressure of about 400 kN m⫺2 before they of water into the tracheal system is prevented. The basal
collapse. Hence, this is an extremely stable plastron that rate of oxygen utilization at 20 °C is about 6 l h⫺1 and
will only be displaced by water at excessive depths. The this is readily provided by the plastron, so that, except in
spiracles open into a series of radiating canals in the poorly oxygenated water, the insect need never come to
cuticle and these connect with the plastron via small the surface.
GASEOUS EXCHANGE IN AQUATIC INSECTS 467
area of anal
opening
closed
+ve
pressure in
branchial
chamber 0
-ve
sternal
up down
movement rest
position
subintestinal
muscle
abdominal
segment 5
abdominal
segment 6
abdominal
segment 7
abdominal
segment 8
1s
Fig. 17.30. Rectal ventilation in a dragonfly larva. Lower traces show action potential frequency in the subintestinal muscle
and in the dorso-ventral muscles of successive abdominal segments. As the dorso-ventral muscles contract they raise the
sterna and compress the branchial chamber and water is forced out. When the subintestinal muscle contracts the sterna are
lowered, pressure in the chamber becomes negative and water flows in through the widely open anus (after Mill & Pickard,
1972).
The plastrons of other insects are generally less the erection of the plastron hairs, as in Elmis (Fig. 17.31c).
efficient than that of Aphelocheirus as they have a less dense The macroplastron is an air store and acts as a physical gill.
hair pile from which the air is more readily displaced. It becomes reduced in size and finally eliminated when the
However, a number of insects with a hair density of insect is submerged, leaving only the plastron. The hairs
3 ⫻104–1.5 ⫻105 mm⫺2 have plastrons that are usually holding the macroplastron are relatively long and flexible,
permanent and adequate for the insect’s needs. In these so that as the gas bubble is reduced they tend to clump,
cases, the plastron is often supplemented by a less perma- leaving patches of exposed cuticle liable to wetting. To
nent macroplastron, consisting of a thicker layer of air avoid this, these insects groom their hair pile and, in Elmis,
outside the plastron and held by longer hairs than the plas- there are brushes on the legs for this purpose. These
tron, as in Hydrophilus (Coleoptera) (Fig. 17.31b), or by brushes are also used to capture air bubbles and add them
468 GASEOUS EXCHANGE
a) Aphelocheirus
opening plastron
cuticle
epidermis
trachea
air
cuticular channel plastron
filaments hairs
cuticle
5 µm
b) Hydrophilus c) Elmis
hairs erect
macroplastron
hairs flattened
plastron
100 µm 20 µm
Fig. 17.31. Plastron. (a) Plastron of Aphelocheirus (Hemiptera). Section through a spiracular rosette showing the junction of a
trachea with a system of channels in the cuticle connecting with the plastron. Below right, detail of the plastron (after Thorpe
& Crisp, 1947a). (b) Macroplastron of Hydrophilus (Coleoptera) (after Thorpe & Crisp,1949). (c) Macroplastron of Elmis
(Coleoptera) showing the hairs erect, forming a macroplastron (above) and with the hairs compressed so that only the true
plastron remains (after Thorpe & Crisp, 1949).
to the macroplastron. Insects that only have a plastron do As a result, water adjacent to an air bubble or a gill will tend
not make grooming movements of this type. to become depleted of oxygen because the rate of diffusion
Review: Thorpe, 1950 into the layer adjacent to the gill surface may not match the
rate at which oxygen is taken into the gill. As movement
17.5.3 Ventilation in aquatic insects into the gill is also a passive, diffusive process, it is obvi-
Close to a solid surface, water movement becomes laminar ously important to maintain the concentration of oxygen
with little mixing between successive layers. The region of in the boundary layer at a high level. This is achieved by
laminar flow is called a boundary layer and, in general, is the insect making ventilatory movements that renew the
greater in depth in still or slowly moving water than in layer of water adjacent to the gill.
fast-flowing turbulent water. This has important conse- In many insects, this is achieved by movements of the
quences for the availability of oxygen at any respiratory gills themselves. In Ephemera a good deal of gaseous
interface. In turbulent water, oxygen is moved by convec- exchange takes place through the gills, but in Cloeon they
tion and tends to be uniformly distributed. Movement function almost entirely as paddles pushing water over
across the boundary layer, however, depends on diffusion. the real respiratory surface on the abdomen. The larva of
INSECTS SUBJECT TO OCCASIONAL SUBMERSION 469
a) Simulium b) Potamodytes
VIEW FROM ABOVE
current
cocoon flow
gills
vortex
air bubble
current
flow VIEW FROM THE SIDE
substratum
Fig. 17.33. Insects in fast-flowing water are oriented with respect to the current. The orientation produces vortices in the
flow. These result in regions of reduced pressure so that gases tend to come out of solution. (a) Pupal cocoon of a blackfly
(Simulium) from above and the side. The orientation of the cocoon in the water current results in the production of vortices
round the gills (after Eymann, 1991). (b) The beetle, Potamodytes, holds on to the substratum facing into the current. The
flow round the legs and body creates regions of low pressure and gases come out of solution to form an air bubble round the
posterior part of the insect (after Stride, 1955).
burrows and crevices where sufficient air is trapped to enable 17.6.1 Spiracular gills
them to survive aerobically for several hours. If they do A spiracular gill is an extension of the cuticle surrounding
become submerged they become quiescent as a result of a spiracle and bearing a plastron connected to the tracheal
anoxia. The time for recovery when returned to air is then system by aeropyles. In water, the plastron provides a large
proportional to the period of anoxia (Evans, Ruscoe & gas/water interface for diffusion, while, in air, the inter-
Treherne, 1971). Lice living on aquatic mammals live in the stices of the gill provide a direct route for the entry of
layer of air trapped in the fur, so that these, too, probably oxygen, and water loss is limited because the gill opens into
encounter no particular respiratory problems (Hinton, the atrium of the spiracle. Thus, in air, water loss through
1976). the spiracles is scarcely greater than in terrestrial insects
The eggs of many terrestrial insects are subject to (Hinton, 1968).
occasional flooding and those of many species have a Spiracular gills occur in the pupal stages of many flies
chorionic plastron (section 14.1.2). A plastron, in the and beetles living intertidally or at the edges of streams.
form of a spiracular gill (see below) is also present on the They also occur in the larvae of a few Coleoptera and in
pupae of many species living in or close to water. By con- Canace (Diptera). Where they occur in pupae, the basal
trast, larval and adult stages living close to water gener- structure of the gill is modified to permit respiration by the
ally lack any specialization of the respiratory system that pharate adult (Fig. 17.34). The spiracular gills of most
would enable them to survive under water, presumably dipteran pupae are prothoracic and connect with the pro-
because they have the means of escaping before they thoracic spiracles. In the cranefly, Taphrophila, for example,
become anoxic. there is a single gill on each side with eight branches (Fig.
Review: Hinton, 1976 – marine insects 17.34a). The whole gill is about 1.5 mm long. Blackfly pupae
INSECTS SUBJECT TO OCCASIONAL SUBMERSION 471
b)
cuticular
bridges
c)
aeropyle
atrium
canal in
cuticle cuticle
of gill
plastron
cavity of gill lines
containing
hemolymph
gill
a) branches
plastron atrium
lines
pupal
cuticle
adult
cuticle
adult
tissue
trachea
Fig. 17.34. Spiracular gills of a pharate adult cranefly (Taphrophila) (after Hinton, 1957). (a) Diagram showing basic
structure and connection of gill to the tracheal system. The two left-hand branches represent the gill as seen from the outside;
the remainder have the upper layer of cuticle removed to show the extent of the atrium. (b) Transverse section through a gill
branch. (c) Detail of a plastron line.
(Simuliidae) also have two prothoracic gills. In this case each The form of the plastron differs in different insects. In
has at least two main branches and in some species there is Eutanyderus (Diptera) and many other species, it is held by
abundant secondary branching. In the pupae of hydrofuge cuticular struts running at right angles to the
Psephenidae (Coleoptera), however, the gills are associated surface of the gill. These struts branch at the apices and
with the abdominal spiracles and in Psephenoides volatilis the branches of adjacent struts anastomose to form an
they are on abdominal segments two to seven. Each gill has open network. An extensive air/water interface thus exists
between four and ten long slender branches. Abdominal in the interstices of the network. In these insects the plas-
spiracular gills also occur in the larvae of beetles of the tron extends all over the gills and connects with the atrium
genera Torridincola, Sphaerius and Hydroscapha. of the spiracle at the base of each gill.
472 GASEOUS EXCHANGE
In Taphrophila, the spiracular atrium extends into each enough to permit efficient absorption of oxygen from well-
gill and its branches, and where the atrium meets the wall of aerated water. As with other plastrons, the plastron of a
the gill it opens to the outside through a series of small pores, spiracular gill resists displacement by high hydrostatic
the aeropyles, about 4 m in diameter (Fig. 17.34b). The pressures.
atrium is flattened in cross-section with the two walls con- Review: Hinton, 1968
nected by cuticular struts so that it does not collapse even if
the gills dry, and the hydrofuge properties of the struts
17.7 GAS EXCHANGE IN ENDOPARASITIC
prevent the entry of water into the atrium. Running from
INSECTS
each aeropyle, on the outside of the gill, is a shallow canal
about 4 m wide which is crossed at intervals of about Endoparasitic insects may obtain their oxygen directly
1.0 m by cuticular bridges about 0.5 m wide (Fig. 17.34c). from the air outside the host or by diffusion through the
The lining of the canals is strongly hydrofuge, so that in cuticle from the surrounding host tissues. In many ichneu-
water each holds a long cylinder of air, known as a plastron monid and braconid (Hymenoptera) larvae, the tracheal
line, which is not easily displaced because of the cuticular system of the first instar is liquid-filled and, even when it
bridges. The plastron lines provide a relatively large becomes gas-filled, the spiracles remain closed up to the
air/water interface over which gaseous exchange occurs. last instar. Thus, these insects and the young larvae of
For the plastron to function efficiently it is important most parasitic Diptera depend entirely on cutaneous
that the gills are turgid when the insects are submerged. In diffusion. In braconid larvae the hindgut is everted
many species of tipulid and in Psephenoides the gills are through the anus to form a caudal vesicle. This is variously
rigid, but in other species turgor is maintained by the high developed in different species, but in some, such as
osmotic content of the gills which results from the hemo- Apanteles, it is relatively thin-walled and closely associated
lymph and epidermal cells which they contain. At the with the heart (Fig. 17.35) so that oxygen passing in is
pupa–adult apolysis the pupal cuticle becomes separated quickly carried round the body. In these insects the vesi-
from that of the adult, but the gills become cut off from the cles are responsible for about a third of the total gaseous
rest of the tissues by a basal occluding membrane so they exchange.
are still lined by an epithelium and contain hemolymph When the tracheal system becomes air-filled, networks
(Fig. 17.34a). The epithelium within the gills disintegrates of tracheoles may develop immediately beneath the
and the cells form loose irregular clusters in the middle of cuticle, thus facilitating the diffusion of gases away from
the gill. This isolated tissue is important because it is able the surface. In Cryptochaetum iceryae (Diptera), a parasite
to repair damage to the surface of the gill, forming cut- of scale insects, there are two caudal filaments, which in the
icular plugs in any holes which are produced, and this third instar larva are ten times as long as the body and are
facility is retained even after the gills have been strongly packed with tracheae. These filaments often get entangled
desiccated. Gill repair is important as a damaged gill loses with the host tracheae and so provide an easy path for
its high internal osmotic pressure and becomes flaccid and oxygen transfer.
inefficient when in the water. Other insects, and particularly older, actively growing
The gills of pupal Simulium are fully expanded in water larvae with greater oxygen requirements, connect with the
as they have an opening at the base into which water can outside air by penetrating the host’s body wall or respira-
freely pass. A thin membrane at the base of each gill in the tory system. The majority of these insects are metap-
newly ecdysed pupa bursts due to the intake of water neustic or amphipneustic, using the posterior spiracles to
resulting from high internal osmotic pressure. This pro- obtain their oxygen. Chalcid (Hymenoptera) larvae are
vides the opening for subsequent water movement into or connected to the outside from the first instar onwards by
out of the gill, ensuring that the shape of the gill is inde- the hollow egg pedicel which projects through the host’s
pendent of the hydrostatic pressures exerted on it. body wall. The posterior spiracles of the larva open into
The efficiency of a plastron depends on its surface area. the funnel-shaped inner end of the pedicel and so make
In spiracular gills the area of the interface varies from contact with the outside air. Many tachinid (Diptera)
1.5 ⫻10⫺4 m2 mg⫺1 net body weight in the pupa of larvae that are parasitic in other insects, tap the host’s tra-
Eutanyderus to 1.9 ⫻10⫺6 m2 mg⫺1 net weight in the cheal supply or pierce its body wall from within using their
pupa of Simulium. These areas are presumably large posterior spiracles. The host epidermis is stimulated to
RESPIRATORY PIGMENTS 473
Within the horse’s stomach, the larva receives only an are no longer available. The hemoglobin thus facilitates a
intermittent supply of air in gas bubbles with the food, and more efficient use of the oxygen supply, but the store it
the hemoglobin of the hemoglobin cells enables the larva provides is very small, lasting, at most, for four minutes
to take up more oxygen than is needed for its immediate (Keilin and Wang, 1946).
requirements. This oxygen is used later when air bubbles
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(Ephemeroptera). Journal of Zoology, 67, 175–89. Patterns of ventilation in dragonfly
Experimental Biology, 40, 455–68. Herreid, C.F., Full, R.J. & Prawel, D.A. larvae. Journal of Experimental Biology,
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caudal lamellae (gills) in a lestid motion. Journal of Experimental Imms, A.D. (1947). Insect Natural
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Imms, A.D. (1957). A General Textbook Lighton, J.R.B. (1996). Discontinuous gas Miller, P.L. (1966a). The regulation of
of Entomology, revised by O.W. exchange in insects. Annual review of breathing in insects. Advances in Insect
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Methuen. Lighton, J.R.B. & Berrigan, D. (1995). Miller, P.L. ( 1966b). The function of
Kaars, C. (1981). Insects – spiracle Questioning paradigms: caste-specific haemoglobin in relation to the mainte-
control. In Locomotion and Energetics in ventilation in harvester ants, Messor nance of neutral buoyancy in Anisops
Arthropods, ed. C.F.Herreid & pergandei and M.julianus pellucens (Notonectidae: Hemiptera).
C.R.Fourtner, pp. 337–66. New York: (Hymenoptera: Formicidae). Journal of Journal of Experimental Biology, 44,
Plenum. Experimental Biology, 198, 521–30. 529–44.
Keilin, D. (1944). Respiratory systems Lighton, J.R.B., Fukushi, T. & Wehner, R. Miller, P.L. (1971). Rhythmic activity in
and respiratory adaptations of larvae (1993a). Ventilation in Cataglyphis the insect nervous system. I.
and pupae of Diptera. Parasitology, 36, bicolor: regulation of carbon dioxide Ventilatory coupling of a mantid spira-
1–66. release from the thoracic and abdomi- cle. Journal of Experimental Biology, 54,
Keilin, D. & Wang, Y.L. (1946). nal spiracles. Journal of Insect 587–97.
Haemoglobin of Gastrophilus larvae. Physiology, 39, 687–99. Miller, P.L. (1973). Spatial and temporal
Purification and properties. Biochemical Lighton, J.R.B. & Garrigan, D.A. (1995). changes in the coupling of cockroach
Journal, 40, 855–66. Ant breathing: testing regulation and spiracles to ventilation. Journal of
Keister, M.L. (1948). The morphogenesis mechanism hypotheses with hypoxia. Experimental Biology, 59, 137–48.
of the tracheal system of Sciara. Journal of Experimental Biology, 198, Miller, P.L. (1981a). Respiration. In The
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ratory water loss. In Environmental F.D. & Johnson, R.A. (1993b). Chapman & Hall.
Physiology and Biochemistry of Insects, Spiracular control of respiratory water Miller, P.L. (1981b). Ventilation in active
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18 Excretion and salt and water regulation
The activities of the cell are carried out most efficiently hindgut (see Fig. 3.1) and lying freely in the body cavity.
within a narrow range of conditions. It is therefore impor- They range in length, in different insect species, from 2 to
tant that the environment within the cell and in the animal 100 mm and from 30 to 100 m in diameter. In most
in general should be kept as near optimal as possible, a insects, they open independently into the gut, but in some
process known as homeostasis. This involves the mainte- species they first come together in groups at ampullae. In
nance of a constant level of salts and water and osmotic crickets, all the tubules open into a single ampulla from
pressure in the hemolymph, the elimination of toxic which a cuticle-lined, tubular ureter connects with the
nitrogenous wastes derived from protein and purine hindgut at the posterior end of the ileum. Malpighian
metabolism, and the elimination of other toxic compounds tubules are absent from Collembola and aphids, and repre-
which may be absorbed from the environment. The excre- sented only by papillae in Diplura, Protura and
tory system is primarily responsible for homeostasis, often Strepsiptera, but are present in all other insects, varying in
following metabolic modification of toxic compounds to number from two in coccids to about 250 in the desert
chemicals more readily excreted or which can be safely locust, Schistocerca. The number may increase during
stored. Some molecules entering the body from the post-embryonic development (see Fig. 15.13). Because of
environment may be too large or too toxic to be dealt with the large number of tubules and the infolding of the basal
by the excretory system and various other tissues may be plasma membrane (see below) their total outer surface area
involved in metabolizing them to less toxic or more readily is large, facilitating an exchange of materials with the
excretable substances. Some insects sequester toxic com- hemolymph. In adult Periplaneta, with more than 150
pounds, isolating them from the major metabolic pathways. tubules, the total outer surface area of the tubules (not
taking account of the infolding of the basal plasma mem-
brane) is over 500 mm2; the infoldings increase the surface
18.1 EXCRETORY SYSTEM
area at least ten times to more than 5000 mm2.
Excretion involves the production of a fluid urine that The wall of the tubule is one cell thick with one or a few
carries potentially toxic materials from the body. This cells encircling the lumen (Fig. 18.1). The principal cell type
process is carried out in two stages: the relatively unselec- in the tubule is produced into close-packed microvilli on the
tive removal of substances from the hemolymph, forming lumen side, while the basal plasma membrane is deeply
the primary urine, and the selective modification of this infolded (O’Donnell et al., 1985). Laterally, the cells are held
primary urine by the resorption of useful compounds or together by septate junctions near their apices.
the addition of others that may be in excess in the body. In Mitochondria are abundant within and immediately beneath
insects, the primary urine is produced by the Malpighian the microvilli and in association with the basal plasma mem-
tubules. Its selective modification usually occurs in the brane. These are the cells which produce the primary urine.
rectum, but may also take place in the Malpighian tubules In many insects, cells that are structurally and func-
themselves or in the ileum. In aquatic insects, epidermal tionally of different types may be intermingled with the
cells outside the gut may also be involved in maintaining principal cells throughout the tubules, or occur in discrete
the insect’s ionic balance. regions so that the tubule is divided into distinct sections.
Review: Bradley, 1985; Razet, 1976 The Diptera, for example, have small stellate cells scat-
tered amongst the principal tubule cells. They have small
18.1.1 Malpighian tubules microvilli which do not contain mitochondria. Mixtures of
Malpighian tubules are long, thin, blindly ending tubes cell types are also known to occur in Periplaneta, Carausius
arising from the gut near the junction of midgut and and Tenebrio.
[478]
EXCRETORY SYSTEM 479
c)
mitochondria
basal
lamina
hemolymph
The Malpighian tubules of Rhodnius have different cell middle section and most mitochondria are concentrated
types in discrete regions of the tubules. The cells in the just below and within the microvilli (Hazelton, Parker &
proximal part of each tubule (nearest the point of origin at Spring, 1988). The distal and middle parts of the tubules
the gut) differ from those in the distal part in having more are both secretory, but their rates of secretion are con-
widely separated microvilli which are variable in length, trolled differently. The short proximal section of tubule is
less complex infoldings of the basal membrane, and mito- probably resorptive (Kim & Spring, 1992). The water
chondria concentrated in the basal region. The Malpighian boatman, Cenocorixa (Hemiptera), has four discrete
tubules of Drosophila also have distinct regions, but, here, regions in its Malpighian tubules (Szibbo & Scudder,
there are also differences between tubules. Posteriorly 1979).
directed tubules have two parts while anteriorly directed The Malpighian tubules of Rhodnius and Lepidoptera
tubules have a short distal section in addition to the main and Diptera in general have no muscles other than a series
and lower (proximal) regions of the posterior tubules. In of circular and longitudinal muscles proximally, while
Drosophila and in Rhodnius, the more proximal parts of the those of Coleoptera and Neuroptera have a continuous
tubules are concerned primarily with resorption, although, muscular sheath. In orthopteroids, Odonata and some
in Drosophila, the same region secretes calcium into the Hymenoptera, strands of muscle spiral round the tubule
tubules (O’Donnell & Maddrell, 1995). (Fig. 18.1). These muscles produce writhing movements
The domestic cricket, Acheta, has Malpighian tubules of the tubules in the hemocoel. This helps to maintain the
with three distinct regions: proximal, comprising about concentration gradients across the tubule wall by continu-
5% of the length of the tubule; mid, 75% of the length; ally bringing them into contact with fresh hemolymph. It,
and distal, 20%. Each region is made up of one cell type. perhaps, also produces fluid movement within the tubules.
The cells of the middle section, forming the bulk of the In some larval Coleoptera and Lepidoptera the distal
tubule, resemble the principal cells described above. Those parts of the Malpighian tubules are closely associated with
of the distal part have close-packed microvilli which the rectum, forming a convoluted layer over its surface.
almost fill the lumen of the tubule, but the basal plasma This is known as a cryptonephridial arrangement (section
membrane is not as extensively folded as in the cells of the 18.4.1.2).
480 EXCRETION AND SALT AND WATER REGULATION
18.1.2 Hindgut of terrestrial insects often perforated. In the mayfly, Coloburiscoides, for
Amongst terrestrial insects, modification of the urine example, it consists only of epicuticle and is less than
often occurs primarily in the rectum which is structurally 0.5 m thick. A thin outer layer of the epicuticle is per-
modified for this function (section 3.1.3). The structure of forated by openings less than 9.5 nm in diameter; the pores
the ileum is not well-known, but, in Schistocerca, the apical in a thicker, inner layer are larger (Filshie & Campbell,
and basal plasma membranes are extensively folded with 1984). Single chloride cells are scattered over the body
large numbers of associated mitochondria, and much fluid surface of larval mayflies (Ephemeroptera) and stoneflies
resorption occurs here (Irvine et al., 1988; Lechleitner, (Plecoptera) and of both larvae and adults of aquatic bugs
Audsley & Phillips, 1989). In this species, the rectum also (Heteroptera).
retains the structure typical of terrestrial insects and In some other aquatic insects, the chloride cells are
contributes to modification of the urine (see Fig. 18.7). grouped together in discrete regions. Larval Trichoptera
In fluid-feeding insects, where water conservation is of have groups of chloride cells forming chloride epithelia on
limited or no importance, the cells of the ileum resemble the dorsal surface of several abdominal segments. In mos-
those just described, but the rectum does not possess the quito larvae, the epithelia form discrete external struc-
usual arrangement of enlarged cells forming rectal pads. tures, the anal papillae (Fig. 18.3). The cuticle covering
these papillae is always very thin, 3.0 m or less, and the
18.1.3 Sites of ion exchange in aquatic insects tips of the short microvilli of the cells beneath are attached
Freshwater insects tend to lose ions to the environment; to it by hemidesmosomes. Folds of the basal plasma mem-
insects in saltwater tend to gain them. Thus, insects from brane extend halfway across the cell. There are many mito-
either environment must compensate for these changes in chondria, indicating that the cells are very active, many of
the ionic composition of the hemolymph in addition to them associated with the bases of the microvilli. The cells
offsetting food-induced changes. They do this by mod- in the papilla appear to form a syncytium, both in mos-
ifying the urine as it passes along the hindgut and by quito and chironomid larvae (Edwards & Harrison, 1983).
moving ions directly out of, or into the surrounding The overall size of these papillae varies inversely with the
medium. ionic concentration of the surrounding water, in at least
In those groups where the hindgut has been examined some species (Fig. 18.3). Their ultrastructure also
in detail, either the ileum or the rectum appears to be asso- changes; the cells have fewer microvilli and mitochondria
ciated with ionic uptake or secretion. In addition, all in insects living in water with higher concentrations of
aquatic insects, whether they occur in fresh or salt water, salts.
possess structures which are known or inferred to be In addition to externally situated chloride cells, at least
involved in ion exchange with the medium. They are some of these insects also have epithelia concerned with
present in the epidermis and may occur as isolated cells or ionic regulation lining parts of the hindgut. For example,
complexes of a few cells, or as more extensive areas. Even in the bug, Cenocorixa, the cells of the ileum have basal and
cells in the gut may be involved in ion exchange with the apical folds with associated mitochondria, but the rectum
medium if the insect drinks or takes in water via the anus. is unmodified. On the other hand, the rectum of fresh-
Because, at least in some cases, it is impossible to deter- water mosquito larvae is lined by a continuous layer of cells
mine the source of fluid in the gut, structures concerned in which both apical and basal membranes are deeply
with modification of the primary urine and those con- infolded and there are many mitochondria. The epi-
cerned with ion exchange with the medium are considered thelium of the anterior part of the rectum also has this
together. structure in saltwater mosquitoes, but the cells of the pos-
Cells that absorb ions from, or secrete them into, the terior rectum are deeper and have more extensive apical
surrounding medium are known as chloride cells, although folding. Most mitochondria are associated with these
they transport other ions in addition to chloride. They are folds. In both fresh and salt water insects, the rectum
characterized by a deeply folded plasma membrane, either usually lacks the complex lateral scalariform junctions
at the apical or basal surface, and mitochondria are abun- between cells that are such a characteristic feature of the
dant, sometimes being closely associated with the folded rectum in terrestrial insects and which are associated with
plasma membrane (Fig. 18.2). The cuticle above the cell is water uptake.
NITROGENOUS EXCRETION 481
cuticle
folds of plasma
membrane
gill
nucleus
mitochondria
basal
lamina
a) distilled water b) 0.006% NaCl c) 0.65% NaCl modified, but the cells of the rectum do not have folded
membranes.
Review: Komnick, 1977 – chloride cells
anal
siphon
18.2 NITROGENOUS EXCRETION
Table 18.1. The distribution of nitrogen in the excreta of insects expressed as a percentage of the total nitrogen in the excretaa
Freshwater insects
Aeschna (L) Odonata 228 ⫺ ⫺ ⫺ 74
Sialis (L) Megaloptera ⫺ ⫺ ⫺ ⫺ 90
Notes:
a Where the total does not equal 100, other components, not shown in the table, make up the balance.
this means that less water is needed for its production. allantoic acid
NITROGENOUS EXCRETION 483
Allantoin is produced in small amounts by many insects, that these are a result of specific elimination from the
but is sometimes present in larger amounts. It is the form hemolymph rather than differential absorption from the
in which most nitrogenous waste is excreted by most midgut. Ommochromes, derived from tryptophan, are
species of Heteroptera that have been studied (Rhodnius is certainly excreted if high levels of tryptophan occur in the
an exception), and by the stick insect, Carausius, and a hemolymph. For example, fecal pellets of locusts are
beetle, Chrysobothris. The larvae of Lucilia accumulate colored red by ommochromes during molting or starva-
uric acid in their tissues, but excrete it after conversion to tion. At these times, tryptophan is probably liberated from
allantoin. Allantoic acid occurs in the excreta of larval and proteins metabolized during structural rearrangement or
adult Lepidoptera. It usually constitutes less than 1% of used in energy production. Ommochromes also color the
the nitrogen excreted by these insects, but may contain as meconium of adult Lepidoptera.
much as 25% of the nitrogen in the meconium. It is also Reviews: Bursell, 1967; Cochran, 1985
produced by larval Hymenoptera and Diptera.
The proportions of these three related compounds, uric 18.2.2 Storage excretion
acid, allantoin and allantoic acid may vary with the food and Waste materials may be retained in the body in a harmless
stage of development. For example, larvae of the grass eggar form instead of being passed out with the urine. This is
moth, Lasiocampa, produce mainly allantoic acid when fed known as storage or deposit excretion. Uric acid, because it
on a grass, but predominantly uric acid when fed on birch. is very insoluble, can be stored as a solid and is found in the
Larvae of the tortoiseshell butterfly, Aglais, produce mainly fat body of many insects at some stages of development.
uric acid; this also predominates in the pupa, but, here, These deposits are not always permanent. For example, in
appreciable amounts of allantoin and allantoic acid are also the cockroach, Periplaneta, uric acid accumulates in the fat
formed. In the adult, allantoic acid predominates. body when there is ample nitrogen in the diet, but this
It is not known how uric acid is transported to the store is depleted if the insect feeds on a diet deficient in
Malpighian tubules. Its insolubility probably requires that nitrogen. It is possible that symbionts are involved in the
it is solubilized, perhaps by binding to a protein. metabolism of the uric acid. In this instance, uric acid pro-
Urea, although present in the urine of a number of vides a nitrogen reserve, but this is probably not common
insects, is usually only a minor component. It is, however, because insects without symbionts probably cannot syn-
the principal component of the nitrogenous excrement of a thesize amino acids from uric acid.
carpet beetle, Attagenus, and the larva of a bruchid seed Some storage of nitrogenous end products must pre-
beetle, Caryedes. The metabolic pathway by which urea is sumably occur in all insects during embryonic develop-
produced in insects is not known, but it is probably inde- ment and, in holometabolous insects, in the pupal stage
pendent of uric acid synthesis. when normal excretion is not possible. For example,
Amino acids are often present in the feces of insects, during embryonic development of the desert locust,
but usually in small amounts that probably result largely Schistocerca, the uric acid content of an egg increases
from incomplete absorption. Under some circumstances, progressively from about 0.5 g egg⫺1 to 25 g egg⫺1.
however, large quantities of amino acids are present. Thus At first, it is present in the yolk, but when the fat body
in the tsetse fly, Glossina, most arginine and histidine from develops it contains much of the uric acid (Moloo, 1973).
the blood of the host are excreted unchanged after absorp- Uric acid also builds up in the fat body of larval Manduca
tion. These are substances with high nitrogen contents when it stops excreting it before pupation (Fig. 18.4).
which would require a considerable expenditure of energy Then, in the days before eclosion, when morphogenesis
if they were to be metabolized along the normal pathways. is almost complete, the accumulation of uric acid
Schistocerca actively secretes proline into the Malpighian increases sharply. Most of it is excreted with the meco-
tubules. It is subsequently reabsorbed in the rectum nium immediately following eclosion (Buckner, 1982;
where it is the principal substrate for oxidative metabo- Levenbook, Hutchins & Bauer, 1971). Uric acid accumu-
lism. lates in epidermal cells of caterpillars and of Rhodnius
There is also evidence that other insects void some during molting. In these cases it is possible that the stores
amino acids in large quantities when they have an abun- simply represent the end product of metabolism of the
dance of nitrogen in the diet (e.g., Zanotto, Raubenheimer individual cells and it is removed when the molt is com-
& Simpson, 1994), but in none of these cases is it certain pleted.
484 EXCRETION AND SALT AND WATER REGULATION
hemolymph
water
K+
-
Cl
solutes -
H+ paracellular
solutes - ATPase
K+ route
transcellular slow movement
route of all solutes
+
uric H
acid
alkaloids
Mg++
SO4
-- tubule lumen
active transport
passive movements
Fig. 18.5. Production of primary urine. Representation of the processes involved in the movement of water into the tubule
and associated transcellular and paracellular movements of solutes (based on Maddrell & O’Donnell, 1992; Phillips, 1981).
which is not actively secreting cations) of Rhodnius about active excretion is induced in the tubules of the variegated
10 times faster than tyrosine (charged) which has a similar grasshopper, Zonocerus by previous exposure to the com-
molecular weight. pound. Locusta, a grass feeder, would not normally
Urate is probably actively pumped into the Malpighian encounter cardiac glycosides, but Zonocerus is highly poly-
tubules of all insects that normally excrete uric acid. In the phagous and probably does (Rafaeli-Bernstein & Mordue,
tsetse fly, Glossina, the activity of the uric acid pump is pro- 1978). Some organic anions that are the end products of
portional to the quantity of urate in the hemolymph. metabolism of aromatic acids are also actively moved into
Subsequently uric acid may be precipitated as the urine is the tubules.
modified on its way to the anus. In adult Calliphora, uric As a consequence of these activities, primary urine
acid is converted to allantoin by the Malpighian tubules contains all the solutes present in the hemolymph, but,
which also actively pump it into the lumen (O’Donnell, except for those compounds that are actively pumped into
Maddrell & Gardiner, 1983). the tubules, their concentrations are lower than in the
Inorganic ions other than potassium and sodium com- hemolymph (Table 18.2). The fluid in the tubule is,
monly diffuse into the urine transcellularly. In adult however, isosmotic with the hemolymph (Table 18.3).
blowflies (Calliphora), the movement of most anions Reviews: O’Donnell & Maddrell, 1983 – transport into the
occurs in inverse proportion to their hydrated size. In tubule; Pannabecker, 1995 – physiology of Malpighian tubules
some insects, however, some of the ions are actively trans-
ported. This is true of phosphate in Carausius and sulphate 18.3.2 Modification of the primary urine
in Schistocerca. 18.3.2.1 Terrestrial insects
Although the passive movement of molecules through The production of primary urine depends on the active
the intercellular gaps is slow, it is important because it movement of potassium or sodium into the Malpighian
ensures that any foreign molecules of moderate size that tubules followed by a passive movement of anions, primar-
enter the hemolymph are slowly removed. This provides ily chloride, to restore electrical equilibrium. The insect
the insect with some capacity to eliminate molecules that cannot normally sustain such a high loss of ions from the
may be toxic and that it may never have encountered before hemolymph and they are recovered by resorption from the
so that specific mechanisms for their safe elimination cannot fluid. In Schistocerca, and perhaps in many other terrestrial
have evolved. Such a mechanism, however, also results in insects eating solid food, this occurs in the ileum and the
the loss of molecules that are important to the insect, such as rectum and depends on the active resorption of chloride
hormones and nutrients. However, lipid soluble com- and sodium (Fig. 18.7). Potassium follows along the electri-
pounds, including some of the hormones, are transported cal potential gradient generated by the movement of chlo-
through the hemolymph bound to proteins. These are too ride (see Fig. 3.26). In Carausius, about 95% of the sodium
large to be lost at any significant rate. Smaller molecules of and 80% of the potassium in the primary urine may be
use to the insect are resorbed at some site downstream of resorbed. On the other hand, the rectum of adult Pieris
that involved in production of the primary urine. shows none of the structures associated with resorption
Some organic molecules with potential toxicity are also which, in this insect, occurs in the ileum (Nicolson, 1976).
actively pumped into the tubules, although the data so far In some other insects, most or all of the resorption
available are sparse. Nicotine and other alkaloids are occurs in the Malpighian tubules themselves. Absorption
actively transported into the urine in Rhodnius, and in of potassium, chloride and water occurs in the lower, prox-
larval Manduca and Pieris. Of these, only Manduca nor- imal regions of the tubules of Rhodnius although the struc-
mally encounters nicotine in its diet and it must be ture of the rectum suggests that some further modification
assumed that the facility in Rhodnius and Pieris reflects the of the urine occurs there.
ability to excrete other compounds. The adults of Useful organic compounds are also recovered from the
Manduca and Pieris cannot excrete the alkaloids, but adults primary urine. Glucose is actively reabsorbed from the
of Calliphora and Musca excrete nicotine after metaboliz- Malpighian tubules of Locusta so the primary urine is
ing it to another compound (Maddrell & Gardiner, 1976). modified even as it is being produced. The uptake of amino
The cardiac glycoside, ouabain, is moved passively into the acids in the rectum may also be active, and this is certainly
Malpighian tubules of the migratory locust, Locusta, but the case with proline in Schistocerca.
URINE PRODUCTION 487
Osmotic
Species Compartment pressureb Na K Cl
Terrestrial insects
Carausius Hemolymph 171 211 218 287
Tubule 171 225 145 265
Rectum 390 228 327 2—
Schistocerca Hemolymph 214 103 212 107
Tubule 226 247 165 288
Rectum 433 221 222 225
Rhodnius Hemolymph 206 174 227 155
Tubule 228 114 104 180
Rectum 358 161 191 2—
Freshwater insect
Aedes aegypti Hemolymph 138 287 223 2—
(larva) Tubule 130 224 288 2—
Rectum 212 224 225 2—
Notes:
a Notice that the osmotic pressure of the tubule fluid (primary urine) is the same as that of the
hemolymph although concentrations of particular ions are different. In terrestrial insects the
rectal fluid becomes hyperosmotic due to resorption of water whereas in freshwater insects it
becomes hyposmotic due to resorption of salts (partly after Stobbart and Shaw, 1974;
Concentrations are in mEql⫺1).
b Expressed as the equivalent solution of NaCl.
living in the Utah Salt Lake which has a salinity equivalent Salt-water insects get rid of excess ions by excreting a
to a 20% sodium chloride solution (3 mol l⫺1 NaCl). urine which is hypertonic to the hemolymph. In salt water
Most of these insects regulate the ionic composition of mosquitoes, some resorption occurs in the anterior
their hemolymph so that its osmotic pressure changes very rectum, but sodium, potassium, magnesium and chloride
little over wide ranges of environmental salinity. This is the ions are secreted into the posterior rectum to create a
case in Aedes detritus and Ephydra, for example (Fig. 18.9). hypertonic fluid (Fig. 18.8b). The osmolarity of the urine
Others, like the caddis fly, Limnephilus affinus, regulate rela- produced in the posterior rectum is proportional to that of
tively poorly but can tolerate a three-fold increase in hemo- the medium. If the insect is in a hypotonic medium, the
lymph osmotic pressure (Foster and Treherne, 1976). posterior rectum is inactive and the insect produces a
Insects living in salt water gain water and salts with hypotonic urine. In this way the hemolymph osmotic pres-
their diet and lose water osmotically. Ingestion of salts can sure is regulated. At least in Aedes campestris, the insect
be limited by selecting food of the lowest available salinity, adapts to the presence of different salts in the medium by
as in Bledius, or by limiting drinking. Limnephilus affinis excreting the appropriate ions. Thus, a larva living in
drinks only 3–7% of its body weight per day compared water with a high concentration of sodium chloride
with about 50% by freshwater insects, but the rate of actively secretes sodium and chloride ions into the poste-
drinking by Aedes taeniorhynchus remains more or less con- rior rectum; if bicarbonate is the dominant anion in the
stant irrespective of the osmotic concentration of the medium it is probably secreted into the rectum; if it is
medium (Bradley & Phillips, 1977a). sulfate, this is secreted into the Malpighian tubules.
URINE PRODUCTION 489
uric
alkaloids acid proline K+
NH 4 HCO 3-
rectum
chloride transport Na +
stimulating hormone proline
K+
active transport
NH 4 passive diffusion
uric
acid
alkaloids excreted
other
toxins
Fig. 18.7. Urine production and modification in a terrestrial insect (Schistocerca). Active transport of potassium into the
Malpighian tubule leads to the osmotic movement of water and most other solutes follow passively. Many of the solutes are
recovered as the urine moves through the hindgut, but ammonia is actively secreted into it. The hormones regulating the
processes are shown in italics (partly based on Phillips & Audsley, 1995).
18.3.3 Control of diuresis changes in the rate of primary urine production that also
The Malpighian tubules of caterpillars appear to secrete necessitate changes in resorption to ensure that an increase
fluid continuously, but, in most terrestrial insects, the rate in fluid loss does not result in excessive loss of ions or other
of urine production varies. Many species reduce urine pro- useful compounds. An increase in the rate of primary
duction and increase blood volume just before a molt and urine production by the Malpighian tubules does not nec-
then increase urine production and rapidly reduce blood essarily result in an increase in water loss as active recovery
volume after cuticle expansion. Diuresis1 is most obvious may occur in the lower part of the system. Individual
at eclosion of adult holometabolous insects. Pieris, for Schistocerca deprived of food for one day, and so subject to
example, reduces its blood volume to less than 33% in the some degree of water shortage, recover about 95% of the
three hours after eclosion, and the blood volume of fluid from the primary urine, and, in the desert beetle,
Sarcophaga is reduced to 25% in 36 hours. Insects that eat Onymacris, the fluid from the Malpighian tubules is
wet food also produce relatively large amounts of urine directed forwards into the midgut and resorbed (Nicolson,
after feeding. This is most marked in blood-feeding 1991). High rates of urine flow may be maintained in these
insects. In the course of a blood meal, Rhodnius may ingest instances to remove potentially toxic materials from the
more than 10 times its own weight; it eliminates most of hemolymph.
the water in the plasma, about half of the ingested volume, Production of the primary urine and subsequent
in the next hour. resorption are regulated independently. A diuretic
These changes in the rates of fluid loss depend on hormone stimulates increased fluid production by the
Malpighian tubules and other hormones regulate
1 Diuresis refers to a rapid flow of urine eliminated from the body reabsorption.
490 EXCRETION AND SALT AND WATER REGULATION
Malpighian tubule
a) freshwater water
(intake by K+
drinking)
Na + Cl - water
Cl -
Cl -
water K+
(osmotic
rectum K+ uptake
through
cuticle Na +
Na +
anal papilla - exchange
with environment
hypotonic
urine
Malpighian tubule
b) saltwater (NaCl) salt and
water
(intake by organic
drinking) compounds K+
SO 4- - Mg ++ Cl - water
HCO 3- Cl -
anterior organic
rectum compounds
K+ Cl -
SO 4- - Cl -
water K+
posterior K+ (loss by
rectum Mg ++ osmosis
through Na +
Na + cuticle)
water
anal papilla - exchange
with environment
30 30
150
20 20
100
%
50 10 10
0 0 0
25 27 31 29 31
number of carbon atoms number of carbon atoms
Fig. 18.12. Effects of epicuticular wax on water loss through the cuticle of adult Drosophila. Larvae were reared at 17 ºC and
pupae maintained at either 17 or 24 ºC. Reduced water loss in the insects from the higher temperature is associated with
higher proportions of longer chain (number of carbon atoms) components of the cuticular surface wax. Amounts of cuticular
components are expressed as percentages of the total epicuticular wax. Only the major constituents are shown (data from
Toolson, 1982).
have greater quantities of cuticular wax than non- Water loss from the respiratory surfaces The respiratory
diapause pupae (see Fig. 15.43) and there is three times as surfaces, being permeable, are a potential source of water
much wax on the surface of the desert beetle, Eleodes in loss. The loss from this source is reduced by the invagina-
summer, when the beetle is exposed to high temperatures, tion of the respiratory surfaces as tracheae and is further
than in winter. If winter beetles are kept at high tempera- limited by the spiracles. When the spiracles are open, the
tures, however, they produce more wax. rate of water loss is increased (Fig. 18.18, and see Fig.
The specific composition of the wax is probably also 17.17). Consequently, conditions which result in more
important. Lipids with longer carbon chains melt at prolonged, or more frequent spiracle opening result in
higher temperatures than those with shorter chain lengths. increased water loss. High metabolic rates due to increased
In Drosophila, insects exposed to higher temperature temperature or activity necessitate longer overall periods
during the pupal period have relatively more long chain of spiracle opening to permit the exchange of respiratory
alkadienes and methylbranched alkanes than insects from gases; they also lead to increased water loss (Fig. 18.13).
pupae kept at lower temperatures. They also lose water This becomes especially important during flight when
less rapidly (Fig. 18.12) (Toolson, 1982). Individuals of the some spiracles may be continuously open. In Schistocerca,
grasshopper, Melanoplus sanguinipes, reared at higher tem- the rate of water loss at 30 °C and 60% relative humidity
peratures have a higher proportion of n-alkanes to methyl- increases from 0.9 mg g⫺1 h⫺1 when the insect is at rest to
branched alkanes of similar chain length than siblings 8.0 mg g⫺1 h⫺1 with the insect in tethered flight. Loss
reared at lower temperatures; n-alkanes melt at higher through the spiracles accounts for a large part of this
temperatures. In this case, rearing temperature has no increase, although not all of it. Discontinuous ventilation
effect on the chain lengths (Gibbs & Mousseau, 1994). has been considered an adaptation to limit water loss,
The ducts of dermal glands and pore canals appear to although not all recent studies support this thesis (section
be the main channels through which water moves through 17.4.3, and see discussion in Hadley, 1994).
the cuticle and the rate of water loss is positively correlated
with the number of dermal glands associated with the Water loss in excretion Nitrogenous excretion necessi-
cuticle. Loss of water by this route may be hormonally tates the production of a fluid urine, and, although some
regulated, perhaps by occluding and opening the channels resorption of water may occur as the urine moves towards
(Machin, Smith & Lampert, 1994; Noble-Nesbitt, 1991). the anus, there is always some water loss. The insect can
494 EXCRETION AND SALT AND WATER REGULATION
flight
pre-flight rest rest
30 warm-up the structure of the alimentary canal is modified so that
water loss (mg.g -1.h-1)
water loss water is shunted directly from the anterior midgut to the
20 hindgut and does not enter the hemolymph (section
3.4.1.1).
40
content of the food is very low, some insects consume
more food than needed in order to extract the water from
20 it. For example, larvae of the flour moth, Ephestia, and
the carpet beetle, Dermestes, eat more food at low humid-
0 ities, but it is clear that the bulk of their water is obtained
0 25 50 as a result of the metabolism of this food rather than
time (minutes) directly from its original water content (see Fig. 18.16).
Some other insects, however, appear to maintain a rela-
Fig. 18.13. Evaporational water loss. Changes in water loss
tively constant nutrient intake irrespective of its water
during pre-flight warm-up and flight of a carpenter bee,
content. Caterpillars, for example, eat more artificial diet
Xylocopa. The increases are mainly due to increased loss through
the spiracles as oxygen consumption increases when the insect
when it is diluted with water, regulating their water
increases its metabolic rate (after Nicolson & Louw, 1982). content by changes in urine production (Timmins et al.,
1988).
control its water loss by regulating the relative rates of Drinking Many insects drink water if they are dehydrated
urine production and resorption. This is demonstrated by in the laboratory and it is assumed that they also do so
differences in the rates of fluid excretion occurring at under natural conditions. For example, locusts without
different times during an insect’s development (section food for 24 hours or with access only to dry food, drink if
18.3.3). A locust feeding on wet food produces feces with a they encounter free water, but turn away from it if they
water content of up to 90%, but this is reduced to 25% have had access to moist food. Cockroaches, termites,
when the insect feeds on dry food in a dry habitat. When beetles, flies, Lepidoptera and Hymenoptera are also
experiencing some degree of water shortage, the insect known to drink (Edney, 1977).
probably reabsorbs as much as 95% of the water in the Some tenebrionid beetles living in the Namib desert
primary urine. obtain water by drinking water that condenses from fogs.
Insects with cryptonephridial systems may be able to They may simply take condensate from any surface, but
resorb water even more effectively. Thus, the larva of some species exhibit behavioral adaptations for collecting
Tenebrio can reduce the water content of its feces to 15%. condensate. Onymacris unguicularis is normally diurnal,
Fluid-feeding insects need to eliminate excess fluid but during nocturnal fogs the insects adopt a head-down
rapidly. In discontinuous feeders, such as Rhodnius, this posture on the tops of sand dunes. Water condenses on the
may be achieved physiologically (see above). Even here, body and trickles down to the mouth, so that insects may
the insect can adjust the loss to its current needs. For increase their weight by as much as 12% overnight (Seely,
example, the percentage of a blood meal eliminated by 1976). Another species, Lepidochora discoidalis, constructs
Glossina just after feeding is reduced in insects which have ridges of sand to trap moisture that it subsequently
previously been desiccated. In phloem- and xylem-feeding extracts (Seely and Hamilton, 1976).
WATER REGULATION 495
Table 18.4. Uptake of water from water vapor. Critical equivalent humidities above
which some insects can absorb water
Critical
equivalent Temperature
Species Order Habitat humidity (%) (°C)
The physiological control of drinking varies in water is in short supply such as deserts, or environments
different insect species. In adult Phormia (Diptera) and the created by vertebrates, but the phenomenon is also exhibited
locust, Locusta, drinking is initiated by reduced blood by a wide range of Psocoptera, including winged adults, that
volume, presumably measured by stretch receptors. live in more moist environments. For most species studied,
However, in the fly, Lucilia, the amount of water imbibed is the critical equilibrium humidity is above 70% relative
correlated with the concentration of chloride ions in the humidity, but Thysanura and several species of biting lice
hemolymph. At least in Locusta, the termination of drink- can take up water even when the humidity is less than 50%.
ing is regulated independently of hemolymph volume, and Water uptake in these insects either occurs in the
is related to the reduction in hemolymph osmotic pressure rectum or through a modified structure on the mouth-
following water intake (Bernays & Simpson, 1982). parts. In tenebrionid beetle larvae, uptake involves the
close apposition of the Malpighian tubules to the rectum, a
Uptake through the cuticle All terrestrial insects passively cryptonephridial arrangement, while in Thysanura and
absorb some water from the air as a result of water mole- the larval rat flea, although the rectum is modified and is
cules striking the surface of the cuticle. The rate of uptake involved in water uptake, it is not closely associated with
increases with humidity (reflecting the number of water the Malpighian tubules. In both these cases, air enters the
molecules in the air) and the permeability of the cuticle. In rectum via the open anus. Water uptake in the desert cock-
most cases, the rate of uptake by this route does not roach, Arenivaga, and in the barklice and biting lice, occurs
balance water loss, but, in some species under some cir- via modifications of the hypopharynx which is extended so
cumstances, there may be a net gain of water. that the structures are exposed between the other mouth-
Some insects and related hexapods have special struc- parts during periods of water uptake.
tures concerned with the absorption of water. The larva of Rectal uptake is most fully understood in tenebrionid
Epistrophe (Diptera) can evert an anal papilla into a drop of beetles. Here the distal ends of the Malpighian tubules are
water and absorb it. In Collembola the ventral tube in close contact with the rectum enclosed by layers of
(Noble-Nesbitt, 1963) and in Campodea (Diplura) the flattened cells that form the perinephric sheath (Fig. 18.14).
eversible vesicles on the abdomen have this function It is assumed that the sheath is impermeable, except perhaps
(Drummond, 1953). at specific points (see below) but anteriorly it is not tightly
A number of insect species actively take up water vapor bound to the rectal wall and hemolymph probably moves
from the air if they are short of water and the air humidity through the gap between the rectum and sheath into the
exceeds a critical equilibrium humidity (Table 18.4). Most of perinephric space immediately surrounding the tubules. At
these insects are larval forms living in environments where intervals, the Malpighian tubules are swollen into flattened
496 EXCRETION AND SALT AND WATER REGULATION
b) Malpighian leptophragma
hemocoel tubule
perinephric
1.0
sheath
perinephric
1.0
4.9 6.8 space
rectal
epithelium
1.1
lumen of rectum
water vapor enters
through open anus
ionic movement
water movement
chambers, called boursouflures. These are so numerous in In caterpillars, which also have a cryptonephridial
larval Onymacris, that they cover the whole surface of the system although they are not known to absorb water
rectum; in larval Tenebrio, they are less extensive. Each vapor, the Malpighian tubules pass beneath the muscle
boursouflure has a cell, called a leptophragma cell, which is layers of the rectum and then double back on themselves
closely apposed to a thin region of the perinephric sheath. to form a more convoluted outer layer. In these insects, the
At these points the sheath may be permeable. cryptonephridial system may be primarily important in
Water uptake from the rectum results from the ionic regulation although it may help to maintain the high
development of a very high osmotic pressure in the blood volume needed for its function as a hydrostatic
Malpighian tubules in the perinephric space. Potassium, skeleton.
sodium and hydrogen ions are all actively transported into In the bark lice (Psocoptera), the hypopharynx bears a
the tubules; chloride ions follow passively. It is believed pair of bladders which are normally concealed by the
that the solution may become supersaturated with potas- labrum and labium. During periods of water uptake,
sium chloride. The osmotic pressure is sufficiently high however, these bladders are exposed (Fig. 18.15) and are
that water molecules are drawn from the air in the rectum covered with a hygroscopic fluid believed to be secreted by
into the perinephric space and then into the tubules (Fig. labial glands. At humidities above the critical equilibrium
18.14b). Water and ions are presumably resorbed into the humidity, water vapor condenses on to the fluid covering
general body cavity in more proximal parts of the tubules the bladders and the condensate is pumped into the gut by
(Machin & O’Donnell, 1991; O’Donnell & Machin, 1991). a cibarial pump (Rudolph & Knülle, 1982). In the desert
WATER REGULATION 497
pump
muscle
dorsal labial
gland
cibarial foregut
pump
retractor
cibarial muscle -
cavity contracted
duct through retractor
hypopharynx hypopharynx muscle -
relaxed
ventral lobe of
labrum hypopharynx
labium ventral lobe of hypopharynx
- covered by secretion of labial
gland
c) water content
1
change in water content
(% of original mass)
-1
-2
-3 pre-experimental reduction in
water content
-4
0 5 10 15 20
time (hours)
Fig. 18.15. Absorption of water vapor via the hypopharynx. (a),(b) Diagrammatic sagittal sections through the head of a bark
louse showing the hypopharynx concealed (a) and exposed (b). In the latter position the distal lobes of the hypopharynx are
covered by a hygroscopic secretion (stippling in b) into which water vapor condenses. The condensed water is drawn through
a duct in the hypopharynx into the gut by the cibarial pump. Arrows show the direction of water movement (after Rudolph &
Knülle, 1982). (c) Regulation of body water in a biting louse. Immediately before the experiment, the louse was exposed to
drying conditions which reduced its water content by 3.5%. At time 0 it was exposed to 91% relative humidity at 30 °C. The
critical equilibrium relative humidity for this species is 52%. The insect absorbed water when the hypopharyngeal bladders
were exposed (arrows, comparable with b above), but slowly lost water when they were concealed (comparable with a above).
Notice that the insect was able to regulate within ⫾1% of its normal water content (after Rudolph, 1983).
cockroach, Arenivaga, the cuticle of the hypopharyngeal and muscular pumping activity, only occur at humidities
bladders is covered by a dense mat of hydrophilic hairs. above the critical equilibrium humidity if the insect’s
Water vapor condenses on to the hairs which swell as they water level is suboptimal. Thus the insect responds both to
take up water. Water is released from the cuticle by a solu- ambient humidity, presumably measured by humidity
tion secreted on to its surface from a gland on the epi- receptors (section 19.7), and its own water content,
pharyngeal face of the labrum (O’Donnell, 1982). perhaps measured volumetrically and involving stretch
The activities associated with water uptake, such as receptors. As a consequence, it is able to maintain its water
opening the anus, exposing the hypopharyngeal bladders, content within narrow limits (Fig. 18.15c).
498 EXCRETION AND SALT AND WATER REGULATION
70% relative 0% relative account for most of the water in the pupa (Fig. 18.16)
humidity humidity (Fraenkel and Blewett, 1944). In order to produce this
80 80 water, these insects eat and metabolize greater quantities
of food at lower humidities. Metabolic water is also of par-
60 60 ticular importance to starved insects and it enables them to
weight (mg)
a) water content
475
water content (µg)
450
metabolic
water
425
water content without
metabolic water
400
0 2 4 6
b) fat content
60
fat content (µg)
80
water content
Table 18.5. Water balance sheet for a locust and Arenivaga under different conditions
(expressed as mg water 100 mg⫺1 day⫺1) (from Edney, 1977)
Locust Arenivaga
Gain
Food 76.05 0.3 ⫺0.22 ⫹0.44
Metabolism 0.9 0.9 ⫺0.87 ⫹0.87
Vapor absorption 0. 0. ⫺0 ⫹2.14
Total 76.95 1.2 ⫺1.09 ⫹3.45
Loss
Feces 32.4 2.4 ⫺0.19 ⫹0.19
Cuticle
Spiracles
6.3
7.35
6.3
2.4 其
⫺
5.43 其
⫹
0.65
Note:
R.H., relative humidity.
absorption of water in the midgut is probably linked to the eggs. In other cases, as in Acheta and Calpodes, the store
salt uptake (Stobbart & Shaw, 1974). In saltwater mosquito probably provides a metabolic reserve (Hazelton et al.,
larvae, the gain in water due to feeding and drinking is 1988; Ryerse, 1979).
greater than that lost through the cuticle and the balance is In the larva of the fly, Arachnocampa luminosa, the
achieved by losing water in the urine. In addition to that in enlarged distal ends of the Malpighian tubules form lumi-
the primary urine, more water is added in the posterior nous organs (section 25.7).
rectum (Fig. 18.8b).
18.6 NEPHROCYTES
18.5 NON-EXCRETORY FUNCTIONS OF THE
Nephrocytes are cells in the hemocoel that take up foreign
MALPIGHIAN TUBULES
chemicals of relatively high molecular weight which the
In a few insect species, the Malpighian tubules are Malpighian tubules may be incapable of dealing with. They
modified for silk production. The tubules of larval take up dyes and colloidal particles but not bacteria. Some
lacewings, Chrysopa (Neuroptera), are thickened distally nephrocytes are usually present on the surface of the heart,
and the nuclei of the cells become branched after the when they are known as pericardial cells, others lie on the
second instar. These thickened regions produce the silk of pericardial septum or the alary muscles. In larval Odonata
the pupal cocoon. During larval life, the tubules produce a they are scattered throughout the fat body and in the louse,
proteinaceous substance that acts as an adhesive on the Pediculus, form a group on either side of the esophagus, in
anal sucker during locomotion and may, at the same time, addition. Nephrocytes of caterpillars form a sheet, one cell
be an excretory end product. Uric acid is stored in the fat thick, in the hemocoel, on either side of the body. The sheet
body of these insects. Antlions (myrmeleontid larvae) also is closely associated with the fat body and extends through
produce silk in the Malpighian tubules and store it in the the thorax and abdomen (Lavenseau, Lahargue & Surleve-
rectal sac. Chrysomelid beetles produce a sticky substance Bazeille, 1981). In larval Cyclorrhapha they form a
in the Malpighian tubules for covering the eggs. conspicuous chain, sometimes called a garland, running
Amongst spittle bugs (Cercopidae, Homoptera) the between the salivary glands (Fig. 18.19a). In addition,
proximal region of the larval tubules is enlarged, consist- larval Calliphora have 12–14 large pericardial cells,
ing of large cells without microvilli. These cells produce 140–200 m in diameter, on each side of the posterior part
the material which, when mixed with air, forms the spittle of the heart, and hundreds of smaller pericardial cells,
within which the larvae live. Some other cercopids build 25–60 m in diameter, around the anterior heart.
rigid tubes, that of Chaetophyes compacta being conical and Nephrocytes are characterized by having their plasma
attached to the stem of the host plant. The proximal part of membrane invaginated to form a labyrinth, but, on the
each Malpighian tubule in this insect is divided into two outside, the folds are held together by desmosome-like
zones, one that produces the fibrils forming the basis of the structures, so that the outer layer of the cell is more or less
tube, and another, more distal zone, that produces spittle. smooth (Fig. 18.19b,c) (Dallai, Riparbelli & Callaini,
Fibrils pass out through the anus and are laid down by 1994). The cells are clothed and held together by a basal
characteristic semicircular movements of the tip of the lamina. Coated vesicles arising from the invaginations
abdomen accompanied by radial pushes from the inside become associated with an intracellular system of tubular
that push the tube into its polygonal form. Other organic elements. Different types of vesicles, including lysosomes
materials and calcium and magnesium from the lie within this zone, while a perinuclear zone contains
Malpighian tubules are deposited on the meshwork of abundant rough endoplasmic reticulum and Golgi.
fibers to form the hardened tube (Marshall, 1965). Nephrocytes usually have one or two nuclei.
Other species also use calcium temporarily stored in The basal lamina and membrane junctions at the outer
the Malpighian tubules for specific functions. For ends of the invaginations limit the size of molecules that
example, in the face fly, Musca autumnalis, and other can enter the labyrinth, but it is known that the nephro-
Cyclorrhapha it contributes to hardening of the puparium cytes of Rhodnius can absorb hemoglobin. Molecules are
(Krueger et al., 1988), and, in Carausius, it is later taken taken into the cell by pinocytosis and, following degrada-
into the hemolymph and deposited in the chorion of the tion, may be returned to the hemolymph. In addition, the
502 EXCRETION AND SALT AND WATER REGULATION
5 m
trachea
coated
vesicle
c)
0.5 m
Fig. 18.19. Nephrocytes. (a) Dissection of the anterior part of a blowfly larva showing the chain of nephrocytes known as a
garland. (b) Nephrocyte from the garland of Drosophila larva. ␣-vacuoles are formed from the amalgamation of pinocytotic
vesicles formed in the labyrinth (after Koenig & Ikeda, 1990). (c) Cortical region of a nephrocyte of Drosophila larva showing the
labyrinth. Arrows show the desmosome-like connections between adjacent projections of the cell (after Koenig & Ikeda, 1990).
nephrocytes release lysozyme which is important in resis- insect producing them and it must have the capacity to
tance to disease (section 5.3.3). prevent autotoxicity. Parasites and predators feeding on
Review: Crossley, 1985 these insects will also be exposed to the potential toxins.
Moreover, as all insects have some innate capacity to
metabolize insecticides, it must be supposed that insects
18.7 DETOXIFICATION
that do not feed on food containing toxins, and do not
Most plants contain chemicals that are potentially toxic to produce their own toxins for defense (section 27.2) have
insects that feed on them. Insects usually respond to such acquired this ability through exposure to naturally occur-
chemicals by avoiding them or by reducing their effects ring toxins which, perhaps, are able to penetrate the
metabolically. This ability is not restricted to plant- cuticle.
feeding insects, however. Many insects synthesize toxins Avoidance of toxins may occur behaviorally; the insect
which are assumed to make them unpalatable to preda- rejects the food on the basis of its odor or taste, or as a
tors. These substances are also potentially toxic to the result of rapid post-ingestive effects (Glendinning, 1996).
DETOXIFICATION 503
Enzyme activity
Notes:
a Larvae of the fall armyworm, Spodoptera frugiperda, were reared on artificial diet without or
with a potentically toxic compound, indole 3–carbinol. The activity of the monooxygenase
system in the midguts of these insects was measured against various potential toxins. Activity
is measured as mmol NADPH oxidized min⫺1 mg⫺1 protein (data from Yu, 1987)
b Compound on which the insects fed.
In other insects, the food may be ingested, but the toxic Many different enzyme systems are known to be involved
chemical is not absorbed so that it never enters the insect’s in these reactions and some systems are almost certainly
cells or hemolymph. ubiquitous. The best known is the system of polysubstrate
The insect’s behavior can also sometimes minimize, or monooxygenases (also called mixed-function oxidases). The
completely negate, the effects of ingested compounds. terminal component of this system is cytochrome P–450, so
This is the case with some compounds, such as the fura- called because it absorbs light maximally at around 450 nm
nocoumarins, that are activated by light. Some insect when complexed with carbon monoxide. Cytochrome
species that habitually feed on plants containing fura- P–450 combines with the substrate (which may be a toxin)
nocoumarins avoid photoactivation of the compounds by and with molecular oxygen, catalyzing the oxidation of the
constructing shelters of leaves or by feeding during substrate. This system is important because the cytochrome
periods of low radiation. Other species have heavily will combine with many different lipophilic substrates and,
melanized cuticles through which light does not penetrate in addition, exists in different forms, called isoenzymes, that
(Arnason, Philogene & Towers, 1992). vary in their substrate specificity. The system is, therefore,
In a majority of insects, however, toxic chemicals that enter able to metabolize a wide range of substances.
the tissues are excreted, often after being metabolized. The The activity of the polysubstrate monooxygenase
changesfrequentlyresultinthecompoundbecominglesstoxic, system towards a particular substrate is usually low or may
but the converse is sometimes true and toxicity is enhanced. not be detectable at all if the insect has not previously
Some compounds, notably those that are water soluble, are encountered the substrate. Exposure of the system to an
metabolized to components that are subsequently incorpo- appropriate substrate, however, induces an increase in
rated into the insect’s primary metabolic pathways. This may cytochrome P–450 leading to more rapid metabolism of
be true of some non-protein amino acids, for example. Most the substrate on subsequent encounters (Fig. 18.20).
lipophilic substances, however, are first converted to a water Because of the broad specificity of the system, it becomes
solubleproductandthenexcretedorsequestered. active against a range of substrates, not just that which
504 EXCRETION AND SALT AND WATER REGULATION
50 50
0 0
c)
LUMEN OF MIDGUT MIDGUT EPITHELIUM HEMOLYMPH LUMEN OF MALPIGHIAN
TUBULE
N N
CH 3 CH 3
N N
nicotine
N
nicotine-1-N-oxide CH 3
N
active
N
O
N
O transport N
O
cotenine-N-oxide CH 3 CH 3 CH 3
N N N
O O O
excreted
Fig. 18.20. Metabolism of a toxic compound (nicotine) by larval Manduca (based on Snyder, Hsu & Feyereisen, 1993; Snyder,
Walding & Feyereisen, 1994). (a) Induction of cytochrome P-450 by feeding on artificial diet containing 0.75% nicotine.
Expressed as amount of P-450 per mg of microsomal protein in the midgut. (b) Rate of metabolism of nicotine in relation to
induction of cytochrome P-450. Expressed as nmol of product formed per mg of microsomal protein in the midgut. (c)
Nicotine is metabolized by the P-450 enzyme to cotenine-N-oxide in the midgut cells. Cotenine-N-oxide enters the
hemolymph and is actively transported into the Malpighian tubules.
caused the induction (Table 18.6). The induction is appropriate enzymes often occurs in the midgut, fat body
temporary, and persists only as long as an inducing agent is and Malpighian tubules with the highest level of activity
present. Some of the other enzyme systems involved in often in the midgut.
metabolizing toxins are also inducible. Different species differ widely in their ability to metab-
These processes may occur in a variety of tissues as olize toxic compounds. Amongst plant-feeding insects,
there is no organ comparable with the liver that is the focus this variation contributes to hostplant specificity. The
for comparable reactions in vertebrates. Activity of the caterpillar of Manduca sexta, for example, habitually feeds
REFERENCES 505
on alkaloid-containing plants, including tobacco, and it is itself, but other species store the defensive substances in
able to do this because it detoxifies the alkaloids. Nicotine glands or in the hemolymph. There is little understanding
from tobacco is taken into the midgut cells where most of it of how these insects avoid autotoxicity, but in the milkweed
is metabolized to cotinine-N-oxide by a microsomal bug, Oncopeltus, and the monarch butterfly, Danaus, that
oxidase (Fig. 18.20c). The cotinine-N-oxide enters the sequester cardiac glycosides, the sodium/potassium
hemolymph and passes into the urine in the Malpighian pumps responsible for maintaining the ionic environment
tubules which have a non-specific alkaloid pump. Any of the nervous system are relatively insensitive to ouabain
nicotine that enters the hemolymph is also rapidly oxi- (a cardiac glycoside). The pumps of insects which do not
dized (Snyder, Walding & Feyereisen, 1994). sequester cardiac glycosides are much more sensitive
Although the end products of these metabolic pro- (section 27.2.5) (Moore & Scudder, 1986).
cesses are commonly excreted, they are sometimes Reviews: Agosin, 1985 – monooxygenases; Brattsten, 1992 –
sequestered. Sequestration may also occur without any metabolic defenses; Brattsten & Ahmad, 1986 – general;
prior metabolism. In some species, the compound is stored Hodgson, 1985 – monooxygenases; Lindroth, 1991 –
in the cuticle, perhaps minimizing the risk to the insect detoxification systems
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19 Thermal relations
Insect systems function optimally within a limited range of their activity produces a significant amount of heat and
temperatures. For a majority of insects, enzyme activity, the thoracic temperatures even of quite small insects are
tissue functioning and the behavior of the whole insect is elevated above ambient during flight. The extent to which
optimal at a relatively high temperature, often in the range thoracic temperature is elevated depends on body size
30–40 °C (see Figs. 3.22, 10.17b). This chapter considers because smaller insects produce less heat and lose it more
the factors that determine an insect’s temperature, how rapidly (Fig. 19.1a), but the relationship between size and
body temperature may be regulated, and how insects cope
with extremes of temperature. a) body weight in bees
50
DEFINITIONS
temperature ( oC)
40
Ectothermal – body temperature depends on heat
acquired from the environment.
30
Endothermal – body temperature depends on heat pro-
duced by the animal’s own metabolism.
air temperature
Heterothermal – body temperature is sometimes deter- 20
mined by the organism’s metabolism (endothermy); at 0 500 1000 1500
other times it is governed by the environment body weight (mg)
(ectothermy).
b) wing loading in dung beetles
Poikilotherm – an animal whose body temperature is vari-
able and dependent on ambient. 40
Homeotherm – an animal whose body temperature is con-
temperature ( oC)
[509]
510 THERMAL RELATIONS
temperature is not a simple one as other factors also affect because heat is lost more quickly as the difference between
rates of heat loss (Stone & Willmer, 1989). For example, thoracic and air temperatures increases.
insects with high wing loading, in general, have higher Because the antagonistic muscles contract almost in
wingbeat frequencies (see Fig. 9.22). This results in more phase with each other, wing movements are very small and
heat production and higher body temperatures (Fig. this warm-up behavior is described as ‘shivering’. In
19.1b). Hymenoptera and Diptera, the wing articulations appear
The flight muscles may be used to generate heat even to become uncoupled so that no wing movements occur at
when the insect is not flying. Because power output for all.
flight for most species is only achieved at relatively high In many insects that exhibit warm-up behavior, the
muscle temperatures, usually above 30 °C, flight at lower thorax is insulated from the abdomen by airsacs or, in
ambient temperatures is preceded by a period of warming Hymenoptera, by the waist (Fig. 19.3a). As a result, heat is
up. Warm-up behavior is especially common in night- not readily transferred to the abdomen except in the
flying insects and those day-flying insects, such as bumble- hemolymph. The heart loops between the dorsal longitu-
bees, that fly early in the year in temperate climates where dinal flight muscles and opens in the head. During its
the ambient temperature, even during the day, is often too passage through the muscles the hemolymph heats up so
low for flight to occur without warm-up. Similar behavior that hot hemolymph is pumped into the head and forced
occurs in some beetles, dragonflies and, occasionally, in back into the abdomen. At the junction between thorax
locusts. Such endothermic warm-up occurs even in some and abdomen (or propodeum and gaster in Hymenoptera),
quite small insects. For example it has been recorded in a this backwardly flowing hemolymph surrounds the aorta
bee, Lasioglossum, weighing only 10 mg, and a hover fly, in which cooler hemolymph from the abdomen is flowing
Syrphus, weighing 20 mg. However, not all insects exhibit forwards. This system functions as a heat exchanger, and
such behavior even though they may be theoretically heat from the thoracic hemolymph warms the abdominal
capable of doing so. For example, horse flies appear to rely hemolymph (Fig. 19.3b). In Apis, the heart forms a spiral
wholly on external sources of heat to produce the body where it passes through the waist. This increases the time
temperatures necessary for flight (Schutz & Gaugler, 1992) and surface area for temperature exchange and so increases
and most Lepidoptera do not exhibit preflight warm-up. the efficiency of the exchanger. Heat is conserved in the
During warm-up, the depressor and levator muscles of thorax by its insulation and the heat exchanger, and the
the wings contract together, instead of in antiphase as they temperature of the abdomen (gaster in Hymenoptera) is
do in flight. This difference results from a change in the usually much lower than that of the thorax (Fig. 19.3c).
pattern of firing of the motor neurons. In the Lepidoptera, Some insects also use the flight muscles to warm up for
with synchronous flight muscles, the motor neurons fire in activities other than flight. The katydid, Neoconocephalus,
phase instead of in antiphase (Fig. 19.2a). Diptera and begins singing soon after dark and will sing at air tempera-
Hymenoptera, however, have asynchronous flight muscles tures as low as 17 °C. The sound is produced by the activity
in which muscle contractions are not determined by the of the wing muscles (section 21.1.2.1). At low tempera-
rate of firing of the motor neurons, but depend on stretch tures, shivering raises the thoracic temperature to 30 °C or
activation of one set of muscles by its antagonists (section above before singing starts. During shivering the muscles
10.5.2). During warm-up, however, the muscles function contract in synchrony, but during singing they act in anti-
as synchronous muscles. At least in the bees, Apis and phase. Some cicadas that sing at night also warm up, pre-
Bombus, the rates of stimulation to the two sets of muscles sumably using the flight muscles to do so (Sanborn et al.,
are not exactly the same so they tend to contract irregu- 1995). In this case, the muscles producing the heat are
larly; the uncoordinated twitches that result are too slow to separate from the tymbal muscles that produce the sound
produce stretch activation. At higher rates of stimulation (section 26.1.3).
the muscles contract tetanically (Esch & Goller, 1991). As Scarab beetles that make dung balls are able to raise
the thorax warms up, the motor neurons fire more rapidly their body temperatures when walking or rolling the dung.
(Fig. 19.2b). This results in a progressive increase in the However, these activities sometimes occur without an
rate of heat production but the rate at which the thorax increase in body temperature so the muscles used in
heats up does not match the rate of heat production walking do not produce the temperature increase. Again, it
BODY TEMPERATURE 511
during warm-up
action potentials.s -1
spike frequency
20
levator
muscle
10
depressor
muscle
0
800
heat production
cumulative heat
production(J)
in flight
levator 400
muscle
depressor
muscle 0
thoracic temperature 35
100 ms (oC) thoracic temperature
25
15
0 5 10 15
time (minutes)
Fig. 19.2. Heat production during warm-up. (a) Activity of the flight muscles of a moth (Manduca). During warm-up, levator
and depressor muscles contract at the same time; during flight they are in antiphase. (b) Warm-up in a bumblebee (Bombus).
Time 0 is the start of warm-up behavior. Muscle activity (shown as spike frequency) increases over time as the thorax warms
up. Notice that the total amount of heat produced, about 800 joules, is sufficient to raise the thoracic temperature by about
200 °C; it does not do so because more heat is lost as the difference between thoracic and air temperature increases. Air
temperature in this experiment was 11 °C. The thorax was already hotter than this at the beginning of the experiment (after
Heinrich & Kammer, 1973).
is likely that heat is produced by oscillations of the flight The extent to which body temperature is raised
muscles (Bartholomew & Heinrich, 1978). depends on the reflectance properties of the insect’s
cuticle. Dark insects, or parts of insects, reflect relatively
19.1.1.2 Heat gain from the environment little of the radiation that falls on them, while light colors
In the absence of solar radiation, the body temperature of a reflect more (de Jong, Gussekloo & Brakefield, 1996). In
resting insect is close to ambient, but solar radiation will relation to this, alpine and arctic insects are often black,
elevate body temperature above ambient. The amount by and many insects of temperate regions exhibit seasonal
which body temperature exceeds air temperature, some- variation in the extent of their black markings. Butterflies
times called the temperature excess, is directly propor- in the genus Colias illustrate these points. Species living at
tional to the intensity of radiation. Small insects heat up high elevations have more dark scales on the underside of
more rapidly than large ones because of their smaller mass, the hindwings and absorb more radiation than those at
but attain a lower final body temperature because they lose lower elevations (Kingsolver, 1983), and Colias eurytheme,
heat more rapidly, having a greater surface/volume ratio which occurs at lower elevations, is darker in the spring
(Figs. 19.4, 19.5). and fall than during the summer. The change is triggered
512 THERMAL RELATIONS
a)
flight muscles -
aorta - hemolymph generating heat airsac -
warmed by heat insulating hairs - forming an
from muscles insulating "fur"
heart - pumps cool
hemolymph forwards
cool hemolymph
in gaster
backwards flow of
hot hemolymph
ventral surface of
waist gaster - no insulation
heat loss
b)
cold hemolymph
warm hemolymph
heart
aorta
ventral
diaphragm
hot hemolymph
moving back
hot hemolymph
hemolymph losing heat to
cold hemolymph in aorta
cool hemolymph
c)
thorax
body temperature ( oC)
40
30 gaster
body temperature = air
temperature
20
10
0 10 20 30 40
air temperature ( oC)
Fig. 19.3. Thermoregulation in a bumblebee (Bombus). (a) Sagittal section of a bee showing the features involved in
regulating thoracic temperature (after Heinrich, 1976). (b) Detail of the heat exchange system in the waist region. As hot
hemolymph flows back under the ventral diaphragm it loses heat to the cool, forwardly flowing hemolymph in the aorta (after
Heinrich, 1976). (c) Temperature of the thorax and gaster of bumblebees in flight. As air temperature rises, the gaster gets
markedly hotter. The insect cannot fly without overheating when thoracic temperature exceeds 45 °C. (after Heinrich, 1975).
BODY TEMPERATURE 513
a)
60 b)
50
reflectance (%)
range of
reflectance
40
50
30
reflectance (%)
20
16 40
daylength
14
(hours)
12
10
30
Mar May July Sept Nov 10 12 14
daylength (hours)
Fig. 19.6. Seasonal variation in black pigmentation of the butterfly, Colias eurytheme (after Hoffmann, 1973). (a) Above:
seasonal variation in the amount of reflectance at 650 nm from the underside of the hind wing. Reflectance is inversely
proportional to the abundance of black scales and so to the degree of heating. Below: seasonal changes in daylength.
(b) Effects of experimental daylengths during the last larval stages on the dark patterning and average reflectance from the
hind wing.
Heat loss from the body is reduced by insulation at the 19.2.1 Behavioral regulation
surface. Many species have the thorax clothed with hairs Extreme temperatures are avoided. At temperatures over
which hold an insulating layer of air round the body. In 44 °C, approaching the upper lethal temperature, larvae of
species of Colias living at high altitudes the hairs are longer the desert locust, Schistocerca, become highly active.
than in species from low altitudes, creating a layer of fur Similarly, movement into an area of low temperature pro-
which, in C. meadii, living above 3000 m, is almost 1.5 mm motes a brief burst of activity. This activity is undirected,
thick. The effectiveness of the insulation depends on the but may tend to take the insect out of the immediately
density of hairs, but, in general, the temperature excess of unfavorable area so that it is neither killed by extreme heat
flying insects is increased 50–100% by their insulation, nor trapped at temperatures too low for its metabolism to
amounting to as much as 9 °C in a large hawk moth. continue efficiently.
Insulation is achieved in dragonflies by a layer of air-sacs Within the normal range of temperature in which they
beneath the thoracic cuticle. are active, insects have a preferred range in which, given the
Review: Prange, 1996 – evaporative cooling choice, they tend to remain for relatively long periods. This
preferred temperature range is towards the upper end of
the normal range of temperatures experienced by the insect
19.2 THERMOREGULATION
and in Schistocerca, for example, extends from 35 to 45 °C
Insects are relatively small animals; the vast majority weigh with a peak at 40–41 °C (Fig. 19.7). The tendency to remain
less than 500 mg. As a result, their surface/volume ratio is still in this preferred range may be regarded as a mecha-
large compared with other, larger animals, and, as a conse- nism tending to keep the insects within a range of tempera-
quence, insects are unable to maintain a constant body tures which is optimal for most metabolic processes.
temperature. Many species can, however, regulate their In the field, many insects are known to regulate body
temperature so as to approximate the optimal under some temperature by moving into areas of sunlight when the air
conditions. This may be done behaviorally, or, in some temperature is low, or moving to the shade when it is high.
cases, physiologically. They also vary posture and orientation to the sun exposing
THERMOREGULATION 515
air
100 40
dorsal
temperature ( oC)
75 abdomen thorax
50
dorsal thorax
25
lateral thorax
0 30
0 25 50 75 0 30
time (minutes) time (minutes)
Fig. 19.8. Cooling by evaporative water loss in a desert cicada (Diceroprocta). (a) Rates of water loss from different parts of
the insect. At moderate temperatures water loss is similar from all parts. When the insect is transferred to high temperature
only a slight increase occurs in loss from the lateral thorax, but much bigger losses occur from the dorsal thorax and abdomen.
Water loss at high temperature occurs primarily through large pores which are present at higher density on the dorsal
abdomen than the dorsal thorax; there are none on the lateral thorax (after Hadley, Toolson & Quinlan, 1989).
(b) The cooling effect of water loss from a feeding cicada (after Hadley, Quinlan & Kennedy, 1991).
the head and thorax are in broad continuity, the thorax is thorax
o
Table 19.1. Mortality of the waxmoth, Galleria, at temperatures above the supercooling
pointa
30 24 226 222
25 27 210 222
20 12–20 260–160 220
15 30–40 100–200 100
10 20 220–50 100
25 20 223–6 100
20 20 221–3 100
⫺5 20 221 100
Note:
a Larvae were reared at 30°C and transferred to the temperatures shown on the second day of
Blattodea
Cryptocercus Adult ⫺6 ? Ribitol
Lepidoptera
Gynaephora Larva ⫺7 ⫺70 Glycerol
Papilio Pupa ⫺20 ⫺30 Glycerol
Coleoptera
Dendroides Larva ⫺10 ? Glycerol, sorbitol
Pterostichus Adult ⫺10 ⫺80 Glycerol
Diptera
Eurosta Larva ⫺10 ⫺50 Glycerol, sorbitol
influenced by many factors controlling the formation of performed by crystals of calcium phosphate in the
ice crystals. Malpighian tubules (Mugnano, Lee & Taylor, 1996).
Reviews: Block, 1990 – cold tolerance; Lee, 1991 – cold Crystals of uric acid may perform a similar function in
tolerance; Sehnal, 1991 – morphogenesis; Storey, 1990 – other insects. As these compounds limit the effects of
biochemistry nucleation occurring round food in the gut, they may be
especially important in species, such as the beetle,
19.3.2.1 Freeze tolerance Phyllodecta, subject to regular nightly freezing, enabling
The supercooling point for most freeze-tolerant insects is them to feed during the day and retain food in the gut at
in the range ⫺5 to ⫺10 °C, although some species super- night. The effects of nucleating agents are not influenced
cool to lower temperatures. Some examples of freeze-tol- by cryoprotectants which may also be present even
erant insects are given in Table 19.2. Once frozen, these though in freeze-susceptible insects these same com-
insects may be able to withstand very low temperatures. pounds act as supercooling agents.
An extreme example is the caterpillar of Gynaephora Glycerol is the most widely occurring cryoprotectant
groenlandica from Greenland. This insect, which freezes at in insects, although other polyhydric alcohols and some
⫺7 °C, can remain frozen for 9 months and survive tem- sugars serve similar functions. These compounds, by
peratures as low as ⫺70 °C. adding to the pool of solute molecules, affect the osmotic
Intracellular ice formation destroys the cells, and if pressure of the hemolymph and help to regulate cell
many cells are affected the insect dies when it thaws. Any volume during extracellular ice formation and also to
mechanism which reduces the rate of cooling at the surface stabilize proteins. They are derived from glycogen
of the cells is important in avoiding intracellular freezing. stored in the fat body and, in many insects, begin to
Thus, the freezing of a large amount of the extracellular accumulate at the onset of an overwintering period (Fig.
body fluids beforehand is beneficial. 19.12). Exposure to temperatures approaching 0 °C is
Ice nucleating agents in the hemolymph or cells often the trigger for the development of cryoprotectants
induce freezing in a controlled way. Ice nucleating pro- and ice nucleating compounds (Fig. 19.13) (Baust,
teins and a lipoprotein are known to occur in the hemo- 1982).
lymph of some freeze-tolerant adult beetles and larval Reviews: Duman, et al., 1991 – ice nucleators; Lee, Lee &
Diptera. Larvae of the goldenrod gall fly, Eurosta, lack ice Strong-Gunderson, 1993 – ice nucleators; Storey & Storey, 1991
nucleators in the hemolymph, but a similar function is – cryoprotectants; Zachariassen, 1982 – ice nucleators
520 THERMAL RELATIONS
a) supercooling point
10 ambient
temperature ( oC)
0
ambient
-10
supercooling
-20 point
-30 supercooling
point
-40
b) cryoprotectants
2000
glycerol
amount (µmol.g -1)
1500
1000
Fig. 19.12. Supercooling points and cryoprotectants of two insects that use different strategies to survive low temperatures
during the winter. Eurosta is a gall fly that tolerates freezing. Epiblema is a gall moth that is freeze susceptible, but has a low
supercooling point. Both species overwinter in the last larval stage in galls on the host plant, and both may occur on the same
plant. Data in the figure relates primarily to insects overwintering near Ottawa, Canada. (a) Variation in supercooling points
over the winter. Ambient temperatures are the minima occurring over a two-week period in one year. Notice that minimum
temperatures are below the supercooling point of Eurosta for several months; the supercooling point of Epiblema is always
well below the environmental minima (based on Morrissey & Baust, 1976; Rickards, Kelleher & Storey, 1987). (b) Seasonal
changes in glycogen and the cryoprotectants, glycerol and sorbitol, that are derived from it. Notice that glycerol levels in the
freeze susceptible insects reach levels five times higher than in the freeze tolerant insect. Epiblema produces very little
sorbitol. Amounts are expressed in relation to the wet weights of the insects (based on Rickards, Kelleher & Storey, 1987;
Storey & Storey, 1986).
inhibited by low
adversely affected by desiccation. Thus, Blatta can survive
temperature, for 24 hours at 37–39 °C if the air is moist, but dies as a
0-5 oC
result of similar exposure in dry air. Humidity does not
affect the lethal temperature of small insects such as lice as
phosphorylase
kinase glycogen
the volume of water available for evaporation is small while
glycogen synthase the surface taking up heat is relatively large.
inactive
glycogen active
For many insects, the lethal temperature for short-term
phosphorylase
uridine diphosphate exposures is within the range 40–50 °C, but, for insects
glucose
from particular habitats, lethal temperatures may be very
phosphorylase glucose-1-
phosphatase phosphate different. Thus Grylloblatta (Grylloblattodea), living at
high altitudes in the Rocky Mountains, dies when its tem-
perature gets as high as 20 °C, while Thermobia
glucose-6-
inhibited by low
phosphate (Thysanura), the fire brat, dies at 51 °C, and for chiro-
temperature, nomid larvae living in hot springs at 49–51 °C the lethal
0-5 oC
temperature must be even higher.
Some modification of the upper lethal temperature
glycerol
occurs, depending on the previous experience of the insect.
Fig. 19.13. Synthesis of glycerol from glycogen. At low Thus Drosophila reared at 15 °C and maintained at 15 °C as
temperatures, the conversion of glycogen phosphorylase from the adults, survive for about 50 minutes in dry air at 33.5 °C,
active to the inactive form is inhibited; the production of the but if they are maintained at 25 °C beforehand they survive
active form continues. As a result, the proportion of this enzyme for about 130 minutes. If the larvae are also reared at the
in the active form is greatly increased so glycogen is metabolized higher temperature the period of exposure that the insects
to glucose-6-phosphate. Other enzymes (not shown) then lead to
can survive is still further increased to 140 minutes in
the synthesis of glycerol or sorbitol. Reconversion of glucose-1-
adults maintained at 15 °C and to 180 minutes in adults
phosphate to glycogen does not occur because the activity of
maintained at 25 °C. Thus two types of acclimation can be
glycogen synthase is inhibited by low temperature.
recognized: long lasting acclimation due to conditions
during development and short-term physiological acclima-
19.4 ACTIVITY AND SURVIVAL AT HIGH
tion depending on the more immediate conditions. The
TEMPERATURES
latter is easily reversible. The effect of physiological
At the upper end of the temperature range, above the pre- acclimation is more marked in dry conditions than in wet.
ferred temperature, insects show a sharp rise in activity. At At least a part of the short-term acclimation to high
still higher temperatures this is followed by an inability to temperatures is a result of the production of heat shock
move, a phase known as heat stupor, and then by death. proteins. These have been demonstrated in several insect
The temperature at which death occurs depends on the species as well as in many other organisms. Drosophila and
species, the duration of exposure and interaction with Locusta each produce six heat shock proteins, and the larva
other factors, in particular with humidity. of the gypsy moth, Lymantria, has seven (Yocum, Joplin &
Insects are cooled by evaporation, so that for short Denlinger, 1991). They belong to three different families
periods they can withstand higher air temperatures if the of proteins with different molecular weights. Some expres-
air is dry. Periplaneta, for instance, dies at 38 °C at high sion of these proteins occurs at normal temperatures, but
humidities, but can survive a short exposure of up to 48 °C expression is enhanced within seconds of a sharp rise in
if the air is dry. Few insects can tolerate the high rate of temperature (Pauli, Arrigo & Tissières, 1992). At high
water loss that cooling necessitates for very long, but some temperatures, proteins become denatured and clump
desert cicadas and honeybees with access to ample water together as insoluble aggregates. Heat shock proteins may
supplies do habitually reduce their body temperatures by protect other proteins so that this does not occur or they
evaporative cooling (see above). may bind to the surface of an aggregate and promote its
For long exposures to high temperature, humidity has dissolution, at the same time causing the proteins to refold.
the opposite effect because at low humidities insects are The same proteins also give some protection against low
CRYPTOBIOSIS 523
a) cuticle b)
peg
dendrites of
hygrosensitive
neurons
dendrite of
thermosensitive
neuron
dendrite sheath
X X
thecogen cell
trichogen cell
tormogen cell
neuron
somata
1 m
axon
Fig. 19.15. Thermohygroreceptor. (a) Diagrammatic longitudinal section through a coeloconic sensillum. (b) Electron
micrograph of a transverse section of a thermohygroreceptor at the level of X–X in (a). Notice the dendrites of two
hygrosensitive neurons and folds of the dendrite of a thermosensitive neuron completely occupying the space in the
dendrite sheath (Bombyx) (after Steinbrecht et al., 1989).
Taphrophila (Diptera) pupae (section 17.6) and Sialis dendrites of both types have a ciliary region. On the basis
larvae can be desiccated for long periods, but when rehy- of their responses, the cells with dendrites extending into
drated show some vital activities such as clotting. the peg are believed to be hygrosensitive, while the cell
which does not enter the peg is probably thermosensitive.
The sensilla may be exposed at the surface of the
19.7 TEMPERATURE AND HUMIDITY
antenna or concealed in a pit, forming one type of coelo-
RECEPTORS
conic sensillum (see Fig. 24.3). When exposed at the
Sense cells responsive to temperature and humidity are surface, they are associated with trichoid mechanorecep-
usually present together in a single sensillum. All insects tors which form a protective umbrella above them, pre-
that have been studied have such receptors on the anten- venting direct contact with any outside object. The
nae. They consist of a short peg without any pores and an number on each antenna is small. There is often a group on
immovable socket. Projecting into the peg are the distal the terminal annulus and one or two on each of the proxi-
dendrites of two neurons (Fig. 19.15). The dendrites mal annuli. Worker honeybees have about 50 on each
usually occupy the whole of the space within the dendrite antenna, and Periplaneta has about 100. Presumably, since
sheath that forms the lining of the peg and are attached to temperature and humidity are ubiquitous properties of the
it. Microtubules within the dendrite are joined together air surrounding the antenna, a large number of receptors is
forming a structure with some resemblance to the tubular not necessary for the insect to obtain accurate information.
body of mechanosensitive dendrites (section 23.1.1.2). A In addition to these sensilla, some multiporous olfac-
third dendrite ends below the base of the peg. In many tory sensilla on the antennae of Periplaneta and Locusta
insects it is produced into a series of lamellae or it may be contain a cell that is thermosensitive. It is structurally
flattened and in the form of a whorl. Proximally, the indistinguishable from the chemosensitive neurons. About
TEMPERATURE AND HUMIDITY RECEPTORS 525
a) b)
action potentials (number.s -1)
100 100
75 75
50 50
25 25
0 0
0 20 40 60 0 20 40 60
time (seconds) time (seconds)
c) d)
action potentials (number.s -1)
100 100
50 50
0 0
0 25 50 0 25 50 75 100
increase in relative decrease in relative
humidity (%) humidity (%)
Fig. 19.16. Responses of hygrosensitive neurons to rapid changes in humidity. (a) Response of moist receptor to a rapid
change from dry (0%) to saturated (100%) air and back again. The firing rate (action potentials s⫺1) increases sharply
immediately following the change and then maintains a higher sustained rate of firing at the higher humidity (cockroach,
Periplaneta) (based on Yokohari & Tateda, 1976). (b) Response of dry receptor to a rapid change from saturated (100%) to dry
(0%) air and back again. The firing rate (action potentials s⫺1) increases sharply immediately following the change and then
maintains a higher sustained rate of firing at the lower humidity (cockroach, Periplaneta) (based on Yokohari & Tateda, 1976).
(c) Response of moist receptor following rapid increases in humidity (stick insect, Carausius). The number of action
potentials is proportional to the magnitude of the increase in relative humidity (based on Tichy, 1979). (d) Response of dry
receptor following rapid decreases in humidity. Note that the x-axis shows the percentage decrease in relative humidity.
Larger decreases produce slightly higher firing rates (stick insect, Carausius) (based on Tichy, 1979).
100 multiporous sensilla with a thermosensitive neuron mechanoreceptors. However, the presumed hygrosensitive
are also present on each maxillary palp of Periplaneta. dendrites in the silk moth, Bombyx, shorten when the
The transduction mechanisms in hygrosensitive insect is dry adapted, suggesting that there may be some
neurons are not understood. One possibility is that direct effect of humidity on the cells (Steinbrecht &
changes in ambient humidity affect the water content of Müller, 1991).
the cuticle associated with the peg causing a small One of the hygroreceptors responds to a rise in humid-
deformation that is perceived by the dendrites connected ity with an increased firing rate, the other responds to a fall
to the inner wall of the peg; they effectively function like in humidity (Fig. 19.16), and they are called moist and dry
526 THERMAL RELATIONS
receptors, respectively. The greater the change in humid- a) response to falling temperature
ity, the higher the firing rate of the cell responding. These 50
10
(number.s -1)
Fig. 19.17. Responses of cold receptor neurons. (a) Response to continuously falling temperature of a cell in a
thermohygroreceptor of the cockroach, Periplaneta. Cold cells in olfactory sensilla respond in essentially the same
way (based on Nishikawa, Yokohari & Ishibashi, 1992). (b) Response to a range of constant temperatures. A cell in a
thermohygroreceptor of Periplaneta is more active at lower temperatures, but cold receptors in olfactory sensilla exhibit only
slight differences with temperature, tending to have maxima at intermediate temperatures (based on Nishikawa, Yokohari &
Ishibashi, 1992). (c) Response to cycling temperature of a cold receptor on the antenna of a beetle larva, Speophyes. The
response follows changes in temperature, increasing as the temperature falls, and decreasing as it rises. Notice that the
temperature changes are slow, only about 0.5 °C over five-minute periods (after Altner & Loftus, 1985).
TEMPERATURE-RELATED CHANGES IN THE NERVOUS SYSTEM 527
-1)
a) temperature
80
action potentials (number.stimulus
input from
sensillum
a)
60
40
20
b)
activity of interneuron
0
20 30 40
temperature ( oC)
b)
action potentials (% change. oC-1)
heated
5
d)
interneuron
heated
time
0
Fig. 19.19. Diagrammatic representations of the response
elicited by a sharp fall in temperature on the activity of four
Fig. 19.18. Effect of temperature on mechanosensory input from different types of unidentified neurons in the cockroach nerve
the wind-sensitive hairs on the head and the activity of a giant cord (after Kerkut & Taylor, 1958).
interneuron in the brain of a grasshopper, Schistocerca americana
(after Miles, 1992). (a) Sensory input (action potentials per
stimulus) from a single hair deflected by 29 m at different Schistocerca and this is, perhaps, a general phenomenon
temperatures. (b) Changes in responses, expressed as percentage (French, 1985; Miles, 1985). The extent of the change
change in the frequency of action potentials for each °C change in differs in sensilla on different parts of the body. For
temperature. Input from the wind-sensitive hairs increased example, the number of action potentials produced by a
sharply when they were heated, but the central response, as standard stimulation of the wind-sensitive hairs on the
indicated by the activity of the interneuron, was dependent on head of Schistocerca more than doubles over the range
the temperatures of both the sensory cells and of the interneuron. 25–40 °C, while changes in the input from sensilla else-
If both experienced a rise in temperature (whole head heated), where on the body are less marked (Fig. 19.18). Hairs on
the interneuron responded sharply to a change in temperature; if
the hind tarsi exhibit a broad maximum of response over
only the temperature of the mechanoreceptors was affected (head
the range 30–39 °C, firing less actively at lower and higher
surface heated), the interneuron showed little change in activity;
temperatures. This corresponds approximately to the pre-
if the temperature of the interneuron increased, but that of the
sensory neurons did not (interneuron heated) its activity ferred temperature range (Fig. 19.7) and these sensilla pos-
increased, but to a lesser extent than if the whole head was sibly provide the insect with information by which it is able
heated. to determine this range when in a temperature gradient.
Changes also occur in the activities of motor neurons
and interneurons. For example, the conduction velocity of
19.8 TEMPERATURE-RELATED CHANGES IN
the motor axon innervating the fast extensor tibiae muscle
THE NERVOUS SYSTEM
of Schistocerca increases with temperature, while the syn-
The rate of firing of peripheral mechanosensory neurons aptic delay between this neuron and the flexor muscle
increases with temperature in both Periplaneta and motor neurons decreases (Burrows, 1989).
528 THERMAL RELATIONS
The firing rate of an interneuron receiving input from the output is inversely proportional to temperature; a
the wind sensitive hairs also increases with temperature, fourth class is not affected by temperature (Kerkut &
and its output is a resultant of its own temperature and Taylor, 1958).
that of the sensory neurons on the outside of the head Thus the response of the insect as a whole is affected by
(Miles, 1992). Within the central nervous system of temperature in a variety of ways; by information from its
Periplaneta, unidentified units, possible interneurons, fall peripheral temperature receptors, by effects on the input
into four categories with respect to their responses to tem- of other types of receptors, and via direct effects on the
perature (Fig. 19.19). In one, the output is directly pro- central nervous system. Changes in internal body temper-
portional to temperature; others show a similar response ature will be slower than peripheral changes, so the central
with the addition of a transient increase if the temperature nervous system will be affected primarily by relatively per-
falls or decrease if the temperature rises; in a third type sistent changes in the external temperature.
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PART V
Communication
The nervous system is an information processing and con- single projection from the soma (Fig. 20.1a). This projec-
ducting system ensuring the rapid functioning and co- tion, or neurite, subsequently branches to form the axon
ordination of effectors, producing and modifying the and dendrite. The peripheral sense cells are bipolar with a
insect’s responses to the input from peripheral sense short, and usually unbranched, distal dendrite receiving
organs. The sensory systems are considered in Chapters stimuli from the environment and a proximal axon extend-
22–24, and the stomodeal system, regulating gut activity, is ing to the central ganglia (Fig. 20.1b). Some multipolar
described in section 3.1.5. This chapter discusses the basic cells, with a number of branches, (Fig. 20.1c) occur in the
structure and functioning of neural elements, and the ganglia of the nervous system and are also associated with
anatomy and functioning of the central nervous system. stretch receptors.
Review: Burrows, 1996 – locust central nervous system The points at which neurons receive information
from, or convey it to other cells are known as synapses. At
most synapses, where transmission from one cell to
20.1 BASIC COMPONENTS another involves a chemical, the plasma membranes of the
two cells lie parallel with each and are close together,
20.1.1 Neuron separated by a gap of 20–25 nm. These chemical synapses
The basic element in the nervous system is the nerve cell, are characterized, when viewed in section with the elec-
or neuron (Fig. 20.1). This consists of a cell body contain- tron microscope, by an area of electron-dense material
ing the nucleus from which one or more long cytoplasmic adjacent to the membrane of the fiber transmitting
projections extend to make contact with other neurons or information, the presynaptic fiber. The dense material,
with effector organs, principally muscles. The cell body is which possibly represents proteins involved in the release
called the soma or perikaryon. It contains abundant mito- of chemical transmitter, forms a patch 150–500 nm across.
chondria, Golgi complexes and rough endoplasmic reticu-
lum. Information is conducted from one cell to another
dendrite
along the processes of the neuron. Usually, one of the pro-
a) monopolar soma
cesses, called the dendrite, is specialized for the reception
axon
of information. It may arise directly from the soma or as a
branch from a major projection of the cell. Input directly
to the soma rarely occurs in insects. The branch of the cell neurite
terminal
which carries information to other cells is usually much arborization
longer than the input branch; it is called the axon. In the b) bipolar soma
axon
central nervous system it is common for both dendrites
and axon to branch extensively; they are said to arborize. dendrite
Golgi complexes and rough endoplasmic reticulum are c) multipolar
absent from the dendrites and axon. No protein synthesis axon soma
occurs in these parts so all organelles and proteins within
them are manufactured in the soma. Numerous micro-
tubules, about 20 nm in diameter, run along the branches,
dendrites
possibly providing pathways for transport of material from
the soma. Fig. 20.1. Neurons. Diagrammatic representation of basic types
Most insect neurons are monopolar, having only a of neuron. Arrow shows direction of conduction.
534 NERVOUS SYSTEM
In the cytoplasm adjacent to the dense material are syn- contain neuropeptides with a modulatory function (see
aptic vesicles (Fig. 20.2a). These are often small, below). The postsynaptic cell has electron-dense material
50–80 nm in diameter, and electron lucent, but may be adjacent to the membrane opposite the presynaptic
larger and electron dense. Sometimes both types are specialization and sometimes, as in Fig. 20.2a, there are
present at a single synapse. The electron-lucent vesicles cisternae.
contain the chemical transmitter that conveys informa- Cells make contact with each other at many synapses.
tion to the following, postsynaptic cell. They release their A single retinula cell in the eye of a fly has about 200
contents into the gap between the cells, known as the syn- output synapses, while some interneurons of the locust
aptic cleft, by exocytosis. The electron-dense granules may have as many as one million output synapses. Often,
BASIC COMPONENTS 535
the output synapses of a cell occur on the branches of the therefore of great importance in determining their electri-
axon, while input synapses are on the dendrites, but, in cal properties (see below).
many neurons, input and output synapses occur on the The glial cells pass nutrient materials to the neurons
same branches (Fig. 20.2b). Sometimes a single output and, at times, contain extensive reserves of glycogen.
synapse communicates with more than one postsynaptic Nutrient transfer is facilitated by finger-like inpushings
cell as in Fig. 20.2a. The number of synapses in a cell is into the neuronal somata. They are relatively much more
not necessarily constant; changes may occur during abundant in neurons with large somata.
postembryonic development and also with the experi- Glial cells have an important function during develop-
ence of the insect. A single neuron typically has input ment of the central nervous system (Tolbert & Oland,
synapses connecting it to more than one presynaptic 1990) and, perhaps, also in making repairs.
neuron and makes output to more than one postsynaptic
cell. Nerve sheath Because nerve activity depends on move-
Some neurons are in direct electrical contact with ment of ions, it is necessary to maintain the immediate
each other, instead of communicating chemically. At environment of the neurons as constant as possible despite
these electrical synapses, the membranes of the two cells the marked differences in ionic concentration that occur
are separated by a gap of only 3.5 nm, and ion channels in between it and the hemolymph. This constancy is pro-
the two membranes link with each other across the gap. vided by a layer of specialized glial cells, known as the per-
This type of connection between cells is called a gap ineurium, round the outside of the nervous system (Fig.
junction. 20.3a).
The cells of the perineurium are held together by tight
20.1.2 Glial cells junctions and septate desmosomes. On the inner side, the
Each neuron is, except for its finest branches, almost cells have relatively extensive processes which penetrate
wholly invested by folds of one or more glial cells. between other glial cells. The perineurium extends over
Synaptic contacts between neurons occur only where the whole of the central nervous system and the larger
glial folds are absent, although the absence of a glial fold peripheral nerves, but it is absent from the finer branches
does not necessarily indicate a synapse. Glial cells are of peripheral nerves where the axons are wrapped round
much more numerous in the central nervous system by individual glial cells. It forms the ‘blood–brain barrier’,
than neurons. Some are closely associated with the allowing the passage only of specific substances into the
somata, others are at the surface of the neuropil with neural environment (see below).
processes extending inward to invest the axons and den- Outside the perineurium is a thick basal lamina
drites. In the case of small axons, several may be known as the neural lamella. It is an amorphous layer of
enclosed within one glial fold (Fig. 20.3a, axon B), but neutral mucopolysaccharide and mucoprotein in which
larger axons are usually completely enveloped. The collagen-like fibrils are present. The fibrils lie parallel
enveloping sheath may consist of a single fold or the fold with the surface, but are otherwise randomly oriented.
may coil round several times so that there are several The neural lamella is probably secreted by cells of the
layers forming the envelope (Fig. 20.3a, axon A). In perineurium, although other cells may also contribute to
general, larger axons are invested by a larger number of it. It provides mechanical support for the central nervous
glial windings. The same effect may be achieved by system, holding the cells and axons together while per-
several overlapping cells. Glial processes are often con- mitting the flexibility necessitated by the movements of
nected to each other by desmosomes, tight junctions and the insect. It offers no resistance to diffusion of material
gap junctions. from the hemolymph into the nerve cord. The per-
Between the glial cells are extracellular spaces. These ineurium and neural lamella are collectively known as the
are relatively extensive in the outer regions of ganglia, but nerve sheath.
much more restricted within the neuropil, where they are Reviews: Carlson & Saint Marie, 1990 – glia; Edwards &
continuous with the narrow spaces between the glial folds. Tolbert, 1998 – glia; Ito, Urban & Technau, 1995 – glial
These narrow spaces show periodic lacunae, which are classification; Lane, 1985 – structure of neurons and glia;
characteristic of insect nerves (Fig. 20.3a). The fluid in the Strausfeld & Meinertzhagen, 1998 – neurons; Treherne, 1985 –
extracellular spaces bathes the neurons directly and is blood-brain barrier
536 NERVOUS SYSTEM
Fig. 20.3. Glia. (a) Diagrammatic section of part of an abdominal ganglion showing glial cells (light shading) that play
different roles. Axons A and B are referred to in the text (after Smith & Treherne, 1963). (b) Representation of the role of glial
cells in maintaining a constant ionic composition of the fluid bathing the neurons in a ganglion. The extracellular
compartment is shown hatched to emphasize its isolation from the hemocoel. The pumps maintain a high concentration of
sodium and low potassium in this compartment despite the diffusive movements of the ions. Broad open arrows indicate
greater permeability to potassium than to sodium ions (after Treherne & Schofield, 1981).
BASIC FUNCTIONING 537
20.2 BASIC FUNCTIONING spike, is of constant amplitude. The first phase of the
action potential is a small increase in permeability of the
20.2.1 Electrical properties of the neuron cell membrane to sodium. As a result, sodium ions flow
A difference in electrical potential is maintained across the into the axon down the concentration gradient and
plasma membrane of a neuron, the inside being negatively produce a small depolarization of the membrane. This, in
charged with respect to the outside. In an unstimulated turn, causes voltage-sensitive sodium channels to open,
cell, this resting membrane potential is often about and this results in a rapid positive swing in the charge on
⫺70 mV. the inside of the membrane, amounting to 80–100 mV in
The membrane potential arises from the differential the cockroach. This is the rising phase of the action poten-
distribution of positively and negatively charged ions tial (Fig. 20.4a). The period of permeability to sodium is
inside and outside the cell. Several factors combine to short-lived because the sodium channels close and are
produce this distribution: a Donnan equilibrium is estab- inactivated. Potassium channels activate more slowly than
lished by non-diffusible organic anions within the neuron; sodium channels, starting to open as the sodium channels
the resting cell membrane is more permeable to potassium close. As a result, potassium flows out of the fiber, which
than to sodium ions; and membrane pumps exchange again becomes more negatively charged on the inside.
sodium ions from the cell for potassium ions outside it in This is the falling phase of the action potential. The total
the ratio 3:2. The net result is that potassium ions are at a duration of the action potential is very brief, only two or
high concentration within the cell, but low outside, while three milliseconds.
for sodium and chloride the converse is true. A current flows in a local circuit away from the point of
Neurons differ from other types of cell in that the depolarization inside the axon, and towards it on the
membrane potential can be varied considerably, and outside (Fig. 20.4b). Where this current reaches an area of
changes in potential provide the signals that enable resting membrane, it produces a slight depolarization,
neurons to communicate with each other. Because the leading to further changes in permeability, first to sodium
resting membrane potential differs from zero, the cell is and then to potassium, that produce an action potential.
said to be polarized. A change in the potential towards This is a continuous process so that the action potential is
zero, a decrease in its negative charge, is called depolariza- propagated along the fiber. Although current flows out
tion; an increase in negativity is called hyperpolarization. from the action potential in both directions, no further
change occurs in the membrane potential of the area
20.2.2 Signal transmission through which the action potential has just passed because
Transmission of signals via the nervous system involves the sodium channels are inactivated and the continued
three different processes. First, the incoming signal, which outflow of potassium negates any tendency for depolariza-
may be visual, mechanical or chemical, is converted to elec- tion.
trical energy (transduction). The transduction mechanisms The number of action potentials produced is propor-
used by sensory cells are considered in sections 22.2.3, tional to the size of the postsynaptic potential (or receptor
23.1.2, 24.1.2 and 24.2.2. The change in membrane poten- potential in the case of sensory neurons). As all the action
tial produced by the incoming signal is called the receptor potentials produced by one neuron have the same ampli-
potential in the case of sensory neurons, or the postsynaptic tude, information about the magnitude of any signal can
potential at synapses within the central nervous system or in only be conveyed in their number and frequency. The fre-
muscles. Second, the electrical signal is conducted along the quency at which action potentials can follow each other is
axon as action potentials; and, finally, the electrical signal is limited by the refractory condition of the axon immedi-
usually converted to a chemical signal for transmission to ately following the passage of an action potential. The
the following cell at the synapse. period for which no further action potentials can be pro-
Review: Pichon & Ashcroft, 1985 duced is known as the absolute refractory period; it lasts
for two or three milliseconds (Fig. 20.4b). After this, an
20.2.2.1 Action potential action potential can be produced, but only by a very strong
Unlike the receptor or postsynaptic potential, which may stimulus (a large receptor potential) and, as the axon recov-
vary in amplitude (see below), the action potential, or ers, progressively weaker stimuli are able to produce action
538 NERVOUS SYSTEM
response response
(action potentials.s -1 )
throughout the cell producing changes in membrane The magnitude of the postsynaptic potential is variable
potential at presynaptic sites that lead to the release of a (graded), and is proportional to the amount of transmitter
transmitter substance, which then acts on a following substance crossing the synapse from the presynaptic termi-
neuron to produce action potentials. The retinula cells of nal. The change in potential induced at the synapse spreads
the eye are of this type, as are some interneurons in the passively, electrotonically, along the dendrite, progressively
central nervous system. The latter are called non-spiking decreasing in amplitude. Action potentials are only pro-
interneurons (see below). The spread of information duced if the change in membrane potential at the action
through the cell is slow compared with that resulting from potential initiation zone, usually near the soma, exceeds a
action potentials, and non-spiking neurons are present in certain magnitude. This change does not depend on the
situations where short-distance communication occurs. activity of a single synapse, but is the sum of all the post-
synaptic events occurring in the neuron; the effects are said
20.2.2.2 Events at the synapse to summate. Summation may be either spatial or temporal.
Chemical synapses The arrival of an action potential at a As contact between any two neurons involves multiple
presynaptic terminal of a chemical synapse results in the synapses, spatial summation is a normal feature of neuro-
opening of voltage-sensitive calcium channels so that nal activity. It may also involve the inputs from more than
calcium ions move into the neuron. Calcium increases the one neuron and the inputs may be excitatory, inhibitory or
probability that a synaptic vesicle, containing transmitter both. Thus, spatial summation may result in an increase
substance, will fuse with the neuronal membrane and (Fig. 20.5b) or a decrease (Fig. 20.5d) in the magnitude of
release the transmitter into the synaptic cleft. The greater the postsynaptic potential, either increasing or decreasing
the number or frequency of arrival of action potentials, the the likelihood that an action potential will be produced by
more calcium enters the cell and the more synaptic vesicles the postsynaptic neuron.
release their contents. Temporal summation results from the arrival of suc-
Each vesicle contains a standard amount of transmitter cessive action potentials at a synapse (Fig. 20.5a). The
so that the release of multiple vesicles increases the amount postsynaptic potential produced by the arrival of a single
of transmitter released in a stepwise manner. The basic action potential at an excitatory synapse may not be big
quantity is called a quantum. Because the release of trans- enough to initiate a new action potential and will slowly
mitter is a probabilistic event, it occurs occasionally even in decay. If, however, a second action potential arrives at the
the absence of any electrical activity in the presynaptic axon. synapse and causes a further depolarization of the postsyn-
The transmitter affects the permeability of the post- aptic fiber before the first potential has completely
synaptic membrane either directly, causing ligand-gated decayed, the total potential resulting from the two succes-
ion channels to open, or indirectly, binding to membrane sive depolarizations is greater than would have been pro-
receptors and activating second messenger systems. The duced by either event by itself. It may exceed the threshold
postsynaptic change may be a depolarization or a hyper- and initiate a postsynaptic action potential.
polarization of the membrane depending on the nature of Depression of the activity of a synapse can also occur as
the transmitter substance and the receptors present on the a consequence of its previous activity (Fig. 20.5c).
postsynaptic membrane. Depolarization is produced by Review: Callec, 1985
opening cation channels in the membrane. As sodium and
calcium ions flow in faster than potassium ions move out, Electrical synapses At an electrical synapse, there is a
the magnitude of the negative charge on the inside of the direct flow of current from the pre- to the post-synaptic
membrane is reduced. Hyperpolarization is produced by cell. As a result, transmission is extremely rapid. Some
an inward movement of chloride ions, increasing the nega- electrical synapses in some animals are known to conduct
tive charge. A depolarization is excitatory; it increases the in either direction, but it is not known if this is also true in
probability that action potentials will be produced. A insects.
hyperpolarization is inhibitory; it decreases the probability
that action potentials will be produced. The changes are 20.2.2.3 Ionic environment of the neurons
known as excitatory postsynaptic potentials (EPSPs) and As the activity of the neuron involves the movement of
inhibitory postsynaptic potentials (IPSPs), respectively. ions into and out of the cell it follows that neural activity is
540 NERVOUS SYSTEM
action
potential
a) temporal summation
5 mV
resting
potential 500 ms
action
potential
b) spatial summation
1 2 1 2 1 2 1 2
5 mV
500 ms
c) decrement of postsynaptic potential
start 5s 15 s 30 s
5 mV
50 ms
d) interaction
EPSP
5 mV
20ms
IPSP
Fig. 20.5. Postsynaptic changes in membrane potential. Each trace shows changes in the membrane potential of the
postsynaptic interneuron following stimulation by the presynaptic neuron. Arrows indicate the arrival of an action potential
in the presynaptic axon. Notice the different time scales. (a) Temporal summation in an interneuron. Stimulation via a single
axon results in a progressive increase in the postsynaptic potential as the intervals between stimuli are reduced. At very short
intervals, an action potential is produced (extreme right) (input from locust tibial mechanoreceptor) (after Newland &
Burrows, 1994). (b) Spatial summation in an interneuron. Stimulation via two separate axons (labelled 1 and 2) produces an
action potential when the stimuli are close together (extreme right) (input from locust tibial mechanoreceptors) (after
Newland & Burrows, 1994). (c) Depression due to previous activity. Continuous stimulation over a 30-second period results
in a progressive decline in the postsynaptic potential. Figure shows the changes in membrane potential of an interneuron at
various times after the start of stimulation (after Newland & Burrows, 1994). (d) Interaction of excitatory and inhibitory
effects. Summation between an excitatory postsynaptic potential (EPSP) and an inhibitory postsynaptic potential (IPSP) is
dependent on the interval between the presynaptic events shown by arrows (cockroach giant interneuron) (after Callec, 1985).
BASIC FUNCTIONING 541
5-hydroxytryptamine
HO peptides
CH 2 . CH 2 . NH 2 FMRFamide
N Phe-Met-Arg-Phe-NH 2
H
proctolin
octopamine
Arg-Tyr-Leu-Pro-Thr-OH
OH
CH.CH 2 . NH 2 see Fig. 21.3 for key
to amino acids
HO
extensive effect, perhaps affecting transmission at a number inhibitory neurotransmitter both in the central nervous
of synapses. This type of secretion is called paracrine release system and at nerve/muscle junctions.
(Fig. 20.7c, d). Other compounds amongst those listed in Table 20.2
may also sometimes function as neurotransmitters, but the
20.2.3.1 Neurotransmitters distinction between neurotransmitter and neuro-
Acetylcholine is probably the most widespread excitatory modulator is not always clear.
transmitter in the insect nervous system (Table 20.2). It is
the major transmitter of olfactory and mechanosensory 20.2.3.2 Neuromodulators
neurons and of many interneurons. Serotonin appears to The synaptic interaction of one neuron with another neuron,
be the neurotransmitter of some chordotonal and multi- or with a muscle, mediated by a neurotransmitter can be
polar sensory neurons (Lutz and Tyrer, 1988), while hista- altered (modulated) by chemicals known as neuro-
mine is the transmitter in retinula cells of the compound modulators. Neuromodulators can act presynaptically, alter-
eyes and ocelli, and dopamine may be a transmitter in the ing the tendency for vesicles of transmitter substance to be
salivary glands. Octopamine functions as a neurotrans- released, or postsynaptically, altering the response of the
mitter in the light organs of fireflies (Christensen et al., postsynaptic membrane to a given quantity of neurotrans-
1983). mitter.
Glutamate is the principal excitatory transmitter at They produce these effects by modifying the ionic
insect nerve/muscle junctions, but also occurs in some permeability of the pre- or postsynaptic cell. Postsynaptic
interneurons. ␥-aminobutyric acid is the principal modulators may compete with a neurotransmitter for
BASIC FUNCTIONING 543
Table 20.2. Substances secreted by neurons in the central nervous system and their
principal functions
Acetylcholine ⫹⫹⫹
(excitatory in CNS)
Biogenic amines
Dopamine ⫹ ⫹
Histamine ⫹
Serotonin ⫹⫹ ⫹
(5-hydroxytryptamine)
Octopamine ⫹ ⫹⫹⫹ ⫹
Amino acids
␥-aminobutyric acid ⫹⫹⫹
(GABA) (inhibitory)
Glutamate ⫹⫹⫹
(excitatory at muscles)
Peptides
Adipokinetic hormone ⫹⫹⫹
Allatotropin ⫹ ⫹
Allatostatin ⫹ ⫹
Cardioactive peptide ⫹⫹⫹
Diuretic peptide ⫹⫹⫹
FMRFamide ⫹
Leucokinin ⫹
Pheromone biosynthesis
(PBAN) ⫹ ⫹⫹
Proctolin ⫹ ⫹⫹⫹ ⫹
Prothoracicotropic
hormone ⫹⫹⫹
Note:
⫹⫹⫹, major function; ⫹, occasional function.
receptor sites on the postsynaptic membrane, or they may The overall effects of neuromodulation may be more
bind to specific membrane receptors, affecting the cell’s profound than changes at single synapses might suggest.
ion channels via second messenger systems. Although such effects have not yet been demonstrated in
Biogenic amines and a number of neuropeptides are insects, in Crustacea a small set of neurons in the stomato-
widely distributed in the central nervous system suggest- gastric ganglion can deliver several different output pat-
ing that they are of considerable importance. In some cases terns depending on the relative amounts of up to 15
they are known to act as neuromodulators, but their func- different neuromodulators released into the system (see
tion is only inferred in a majority of instances. There are, Harris-Warwick et al., 1992).
as yet, no well established cases of neuromodulatory effects Homberg (1994) describes the distribution of ‘neuro-
in the nervous system in the intact insect, but experimental transmitters’ (including neuromodulators) in the insect
work demonstrates the types of effects to be expected. brain.
544 NERVOUS SYSTEM
vesicle of
vesicle of receptor for neuromodulator
neurotransmitter receptor for
neurotransmitter neuromodulator
neurotransmitter
receptor for
neuromdulator
terminal of separate
neuron containing
neuromodulator
Fig. 20.7. Neuromodulation at a synapse. Diagrammatic representation of different pathways by which neuromodulators
may affect the postsynaptic element. Transmitter compound is shown as black triangles; neuromodulator as shaded hexagons.
(a) A synapse with no neuromodulators. (b) Parasynaptic secretion. The neuromodulator co-occurs with the transmitter and
acts close to the synapse. (c) Paracrine secretion. The neuromodulator co-occurs with the transmitter but is released round
the area of the synapse. It may affect other neurons in the vicinity. (d) Paracrine secretion. The neuromodulator is produced
by a separate neuron and affects the general environment around the synapse.
Octopamine Octopamine probably has a widespread increase is responsible for a change in the properties of
modulatory effect on the activity of skeletal muscles the cell membrane of the interneurons (Orchard,
(see section 10.3.2.4), but it also modulates the activity Ramirez & Lange, 1993).
of some interneurons and sensory neurons. One Octopamine may also act via the hemolymph as a
example of its effect on interneurons concerns the neurohormone modulating the activity of sensory
generation of the pattern of activity of locust flight neurons. This occurs with the neuron of the locust
muscles. During flight, the interneurons produce action forewing stretch receptor. Its activity is enhanced by
potentials in bursts (Fig. 20.8a), but a similar bursting octopamine (Fig. 20.8b) which is released into the hemo-
pattern cannot be generated experimentally when the lymph at the beginning of flight.
insect is at rest unless octopamine is applied to the In locusts, the dorsal and ventral unpaired median cells
preparation. It is known that the concentration of in the thoracic and abdominal ganglia and some inter-
octopamine in the metathoracic ganglion increases neurons in the brain are octopaminergic (Stevenson et al.,
during the early part of flight, and it is likely that this 1992).
BASIC FUNCTIONING 545
20
understood except for those that are neurohormones. One
exception is proctolin which functions as a neuromodulator
at some visceral and skeletal muscle junctions (section
10.3.2.4). Nässel & O’Shea (1987) report about 500 procto-
10
linergic neurons, both interneurons and motor neurons, in
various parts of the central nervous system of Calliphora.
20.2.3.3 Neurohormones
0
0 5 10 15 Neurohormones are produced by neurons in various
time (minutes) ganglia of the central nervous system. Their distribution
Fig. 20.8. Neuromodulatory effects of octopamine in the locust. (a) Effect on an interneuron associated with the
flight muscles. When the insect is in flight the action potentials in the interneuron occur in bursts, but stimulation of
the interneuron in a quiescent insect produces a train of action potentials. A bursting pattern similar to that occurring in
flight can be produced experimentally by applying octopamine to the quiescent preparation (after Orchard, Ramirez &
Lange, 1993). (b) Output from a wing stretch receptor with the wing oscillating at 18 Hz (similar to the normal wingbeat
frequency). When octopamine was added the output from the stretch receptor increased for a time (after Ramirez &
Orchard, 1990).
546 NERVOUS SYSTEM
a) Dictyopterus b) Musca the same body segment. The number of motor neurons in
each ganglion is relatively small, corresponding to the rela-
brain brain tively small number of muscle units that insects possess;
subesophageal subesophageal
ganglion ganglion nevertheless, there are about 500 in the mesothoracic gan-
compound glion of Periplaneta.
thoracic ganglion
ganglia The somata of motor neurons are relatively large; in
(thoracic +
abdominal) the locust metathoracic ganglion they range from about 20
to 90 m in diameter. They are roughly constant in posi-
tion and homologous neurons on the two sides of a gan-
glion are placed more or less symmetrically. Somata of
abdominal axons running within a single nerve tend to be grouped
ganglia
together, but even those running to the same muscle can be
widely separated. For example, the somata of the fast and
slow axons to the metathoracic extensor tibiae muscle are
widely separated and their axons run in different nerve
Fig. 20.10. Numbers of ventral ganglia (from Horridge, 1965). branches.
(a) Most ganglia remain separate (Dictyopterus, Coleoptera). (b) The neurite of each motor neuron increases in diam-
All the ventral ganglia except the subesophageal are fused into a eter on entering the neuropil, within which it gives rise
single compound ganglionic mass (Musca, Diptera). to many branches (Fig. 20.11). The shape of this den-
dritic tree is characteristic of each motor neuron and its
larval or adult insects is eight, as in Thysanura, male Pulex complexity an indication of the complexity of its syn-
(Siphonaptera) and many larval forms, but the last gan- aptic connections with other neurons. The axon
glion is always compound, being derived from the ganglia branches from the neurite and runs, unbranched (except
of the last four abdominal segments. for those in the median nerve), into one of the peripheral
The abdominal ganglia are smaller than those of the nerves.
thorax and, in general, fewer peripheral nerves arise from
each of them than arise from the thoracic ganglia. In addi- 20.3.2.2 Interneurons
tion, the branching of the nerves is less diverse and vari- Direct synaptic connections are known to occur between
able, reflecting the relative simplicity and similar afferent (sensory) fibers and motor neurons, but these
segmental organization of the abdominal musculature. monosynaptic pathways are unlikely to occur commonly
Sometimes, most or all of the ventral ganglia are fused because this arrangement allows for little variability of
to form a single compound ganglion as in the blood- response. In general, interneurons are interpolated
sucking bug, Rhodnius, and in cyclorrhaphan flies (Fig. between sensory and motor neurons, and most of the
20.10b). Adult holometabolous insects often have more neurons in the central nervous system are interneurons.
ganglia fused than the larvae (see Fig. 15.23a), but the Anatomically, interneurons can be divided into local
cyclorrhaphous Diptera are an exception. and intersegmental interneurons. Local interneurons are
In most cases the muscles of a segment are innervated restricted to a single ganglion; they may be spiking or
by neurons from the ganglion of the same segment, but non-spiking. It is estimated that there are approximately
some innervation by axons arising in neighboring ganglia 1500 intraganglionic interneurons in the mesothoracic
also occurs (see Fig. 10.8). Some afferent fibers may also be ganglion of Periplaneta compared with 200 inter-
intersegmental (see below). ganglionic interneurons. Non-spiking interneurons form
Reviews: Altmann & Kien, 1987; Weevers, 1985 a significant proportion of these local interneurons, at
least in the thoracic ganglia. For example, in the meta-
20.3.2 Neurons of the central nervous system thoracic ganglion of the locust about 100 non-spiking
20.3.2.1 Motor neurons neurons are recognizable compared with about 140
Each segmental ganglion contains the somata of motor spiking local interneurons, but many other neurons
neurons concerned with control of muscles, primarily in remain to be characterized.
548 NERVOUS SYSTEM
connective to first
abdominal ganglion
b)
membrane potential in
non-spiking interneuron
action potentials in
motor neuron 1
action potentials in
motor neuron 2
Non-spiking local interneurons Non-spiking local inter- low to produce a tonic postsynaptic potential. This may be
neurons in the ventral ganglia often arborize extensively in depolarizing, so that the postsynaptic fiber fires tonically, or
the ipsilateral side of the ganglion (that is, on the same side as hyperpolarizing, so that the activity of the postsynaptic fiber
the soma) (Fig. 20.12a). Slow changes in membrane poten- is inhibited. Changes in the membrane potential of the non-
tial are adequate to produce synaptic transmission; spike spiking neuron lead to graded changes in postsynaptic
production does not occur. Non-spiking neurons have low potential and hence to changes in the rate of spike produc-
resting potentials, of about ⫺30 to ⫺50 mV, compared with tion in the postsynaptic fiber (Fig. 20.12b). An experimental
spike-producing neurons (about ⫺70 mV). Postsynaptic change in the membrane potential of as little as 2 mV may
potentials are produced by these neurons by the release of a have such an effect, and, in the course of normal activity,
chemical synaptic transmitter just as in spiking neurons, and changes of up to 15 mV can occur.
in some cases the resting membrane potential is sufficiently Review: Siegler, 1985
ANATOMY OF THE NERVOUS SYSTEM 549
Interganglionic interneurons Interganglionic inter- tibiae muscle and the common inhibitor of the leg muscula-
neurons transmit information along the nerve cord. Fibers ture (see Fig. 10.9). It also provides inhibitory input to the
that carry information from anterior to posterior ganglia coxal adductor muscle motor neuron.
are called descending fibers; those transmitting informa- The ventral nerve cords of cockroaches, various
tion to the brain or anterior ganglia are called ascending Orthoptera, dragonfly larvae, Drosophila (Diptera) and
fibers. These neurons are responsible for co-ordinating the possibly all insects contain a number of axons which are
activities of different ganglia and so bring about the coor- much bigger than the majority. They are called giant fibers.
dinated activity of the whole insect. The axons of these In the cockroach, there are six to eight giant fibers,
neurons may have arbors, indicating that they make syn- 20–60 m in diameter, in each connective as well as 10 to
aptic connections, in several ganglia or may extend 12 medium-sized axons between 5 and 20 m in diameter.
through some ganglia without branching, arborizing only (The axons of most interneurons are less than 5 m in
in the ganglion where they end. diameter). In the cockroach, the somata of all the giant
One of the most thoroughly studied interganglionic fibers are in the terminal abdominal ganglion. In contrast,
interneurons is the descending contralateral movement adult Drosophila have only two giant interneurons and they
detector (DCMD) of the locust. There is one DCMD in have somata in the brain.
each neural connective, running from the brain to the Giant fibers run for considerable lengths of the nerve
metathoracic ganglion. The soma lies posteriorly in the cord. In Periplaneta the largest fibers extend from the ter-
protocerebrum. Within the brain, the axon swells to form minal abdominal ganglion to the subesophageal ganglion.
an integrating segment from which six or more major den- Within the terminal abdominal ganglion each giant fiber
drites diverge so that their fine branches occupy a sphere has an extensive dendritic arborization within which syn-
about 200 m in diameter. The neuron receives input from apses are made with afferent fibers from the cercal nerve
other neurons in this region. In particular, it receives (Fig. 20.14). Different giant fibers arborize in different
information about small-scale movements in the visual parts of the ganglion suggesting that they receive input
field. Beyond the integrating segment, the axon crosses to from different groups of sensilla.
the contralateral side of the brain and then passes down the The giant fibers allow for the rapid transmission of
ventral connective to the metathoracic ganglion. It gives information over long distances because of their high
rise to a single branch in the prothoracic ganglion, and to conduction rates due to their large size and lack of syn-
further branches in both the mesothoracic and meta- apses.
thoracic ganglia. These branches form less extensive arbor-
izations than the dendritic fields of the motor neurons with 20.3.2.3 Homologies
which they connect. The neuron makes excitatory output Because the early patterning of neurogenesis is similar in
synapses to a number of motor neurons, some of which are different segments and even in different insects, it is some-
shown in Fig. 20.13. These include neurons of the extensor times possible to recognize homologous neurons in different
550 NERVOUS SYSTEM
b) midline of
ganglion
a)
giant axon
giant axon
neurite
neurite site of spike
soma initiation
soma
dendritic tree
dendritic of giant fiber
tree
inhibitory local
interneuron interneurons
sensory axons in
excitatory synapse ipsilateral cercal
inhibitory synapse nerve
Fig. 20.14 Integration at synapses. A giant fiber in the terminal abdominal ganglion of Periplaneta (after Callec, 1985). (a)
Diagram showing the dendritic arbor and contralateral position of the soma. (b) The neuron with the giant axon receives
direct input on to its dendritic branches from sensory neurons in both the ipsilateral and contralateral cerci as well as from
local interneurons. Inputs are both excitatory and inhibitory.
ganglia and even in different insect species despite the efferent axons, but the antennal and cercal nerves contain
differences that develop postembryonically as a consequence only sensory axons.
of functional differentiation. For example, specific inter- A small median nerve which runs from the posterior
neurons in the meso-, metathoracic and first abdominal end of each ganglion lies between the paired connectives
neuromeres of the locust that have somewhat similar joining the ganglia. In the abdomen, it extends from one
arrangements of their axons and arborizations (Fig. 20.15) ganglion to the next, but, in the thorax, it extends only part
develop from precisely homologous cells during early of the way before branching transversely to the spiracles
development. In other cases, where the embryonic origins and some ventilatory muscles. These nerves contain small
are not known, possible homologies are suggested by the numbers of sensory and motor axons. Each motor axon
similarity of position and anatomy of neurons, sometimes divides where the median nerve branches, so that the
together with their immunocytochemical characteristics. homologous muscles on either side of the body are inner-
Review: Kutsch & Breidbach, 1994 vated by the same neuron (see Fig. 17.21).
circumesophageal
connective labral nerve
frontal connective
b) lateral
ocellus
compound
eye
protocerebrum
median ocellus
nervi corpora
cardiaci
antennal nerve
corpus
cardiacum
deutocerebrum
hypocerebral
tritocerebrum ganglion
aorta inner
esophageal
nerve
recurrent nerve
corpus allatum
frontal ganglion
esophagus
frontal connective
outer esophageal
labral nerve nerve
postesophageal circumesophageal
commissures connective
number of fibers in the peduncle increases less in flies kept system connect in the collar. The mushroom bodies of
in isolation compared with those in a crowd, while, other insects do not have these visual connections.
amongst Apis workers, the lip and collar of the calyx Another group of neurons, known as feedback
increase more in foragers compared with nurse bees of the neurons, arborize in both the lobes and the calyx (Fig.
same age (Fig. 20.19b,c) (Durst, Eichmüller & Menzel, 20.18d). The terminals of the Kenyon cells converge
1994). on to a number of large output interneurons in the
In all insects, the mushroom bodies receive input lobes. These interneurons run primarily to other parts
from neurons carrying information from the antennal of the protocerebrum, perhaps including the central
lobes (Fig. 20.18b). Within the calyx, each of these body (Fig. 20.18c).
neurons communicates with a large number of The mushroom bodies are involved in olfactory, and,
Kenyon cells. In Apis, these connections are made in perhaps, in some insects, visual learning.
the lip of the calyx while inputs from the visual Review: Schurmann, 1987
BRAIN 553
antennal lobe
circumesophageal
connective tritocerebrum
postesophageal
commissure
20.4.1.2 Central complex There are no direct connections between the central
The central complex is a series of interconnected neuro- complex and the corpora pedunculata, or the optic or anten-
pils in the center of the protocerebrum. The principal fea- nal lobes, and the functions of the central complex are not
tures are the protocerebral bridge, the central body and understood. As it is the only unpaired region of organized
lateral accessory lobes (Fig. 20.20a) although different ter- neuropil it is probably concerned with the integration of
minology has been used in different insects (see Homberg, information from the right and left halves of the brain.
1987). The arrangement of neurons within the complex is Review: Homberg, 1987
well-ordered. One conspicuous feature is an array of 64
axons arising from somata in the protocerebrum and 20.4.1.3 Optic lobes
running in bundles of four through the central body. The optic lobes are lateral extensions of the proto-
These axons arborize extensively in the protocerebral cerebrum to the compound eyes. Each consists of three
bridge and in the central body and some also extend into neuropil masses (Fig. 20.17), known as the lamina, the
the lateral accessory lobes. In parallel with these fibers, medulla and the lobula complex which, in Lepidoptera,
although innervating different parts of the complex, is a Trichoptera and Diptera, is subdivided into the lobula and
second series which are serotonergic (Homberg, 1991). the lobula plate. Within these masses, the arrangements of
Others, arising from somata lying both dorsally and ven- arborizations of different sets of neurons produce a layered
trally to the complex, run transversely through the central appearance. Between successive neuropils the fibers cross
body, arborizing in its upper or lower parts (Fig. 20.20b,c). over horizontally forming the outer and inner optic chias-
In addition to these intrinsic fibers of the central complex, mata so that the neural map of the visual image is reversed
many others convey information to and from the system. and then rereversed.
These enter it via the protocerebral bridge or make direct In the lamina of most insects, the axons of retinula cells
connections between the central body and the anterior and from one ommatidium remain together and are associated
posterior protocerebrum. Some of the probable input with neurons originating in the lamina and the medulla to
fibers are serotonergic and have extensive arborizations in form a cartridge. In insects with an open rhabdom (section
one or another part of the central complex. Most of the 22.1.2), however, each cartridge contains the axons from
cells of the central body contain neuropeptides, probably retinula cells with the same field of view rather than from
used as neurotransmitters, and many of the transverse the same ommatidium. In either case, the number of car-
neurons innervating the lower part of the central body are tridges in the lamina is the same as the number of omma-
GABAergic. tidia.
554 NERVOUS SYSTEM
lip
Kenyon
cells 3 collar
2 calyx
basal
ring
calyx
1
α lobe
peduncle β lobe
peduncle α lobe
antennal
lobe
β lobe glomerulus
soma
lateral
protocerebrum
Fig. 20.18. Mushroom body. Examples of neurons associated with the mushroom bodies. (a) Intrinsic neurons (Kenyon cells:
labelled 1, 2 and 3) showing different types of dendritic arborization in the calyx. Notice that the axon of neuron 1 extends
only into the  lobe; for neuron 2, only the proximal part is shown; the axon of neuron 3 extends to both the ␣ and  lobes
(Apis) (based on Mobbs, 1985). (b) Input neuron from the antennal lobe. The dendritic arbor is restricted to a single
glomerulus, but this is not true of all the input neurons from the antennal lobe to the mushroom bodies. (Notice that this
would be called an output, projection neuron from the antennal lobe, but an input neuron to the mushroom body). The axon has
branches to both parts of the calyx (Manduca) (based on Homberg, 1994). (c) Output neuron with a dendritic arbor in the ␣
lobe and an axon running to the lateral protocerebrum (Manduca) (based on Homberg, 1994). (d) Feedback neuron
connecting different parts of the mushroom body (Manduca) (based on Homberg, 1994).
BRAIN 555
a)
Orthoptera Schistocerca peduncle and lobes
Mantodea Mantis calyx
Blattodea Blaberus
Isoptera Zootermopsis
Macrotermes
Lepidoptera Pieris
Diptera Chrysops
Hymenoptera Rhogogaster sawfly
Andrena solitary bee
Apis honeybee
Vespa social wasp
0 50 100 150
relative volume (%)
b) Drosophila c) Apis
3000
normal females 60
number of fibers
2500
40
2000 20
0 10 20 30 40 50
days after eclosion
0
normal males newly nurse forager
males - no odor eclosed
females - no odor
lip of calyx
females - isolated
collar of calyx
basal ring of calyx
peduncle and lobes
Fig. 20.19. Mushroom bodies. Variation in development. (a) The volumes of the mushroom bodies in different species of
insect expressed relative to the size of the central complex. The mushroom bodies are relatively much larger in social insects
than in others. Notice that in termites (Isoptera) the peduncle and lobes account for most of the volume whereas in the
Hymenoptera the calyx contributes the greater part (after Howse, 1974). (b) Changes in the number of fibers (thought to
reflect the number of Kenyon cells) in the peduncle of a mushroom body of Drosophila. The insects shown by histograms
were all 21 days post-eclosion. Maintenance in environments offering less stimulation resulted in smaller numbers of fibers in
both males and females (after Technau, 1984). (c) Changes in the volumes of parts of the mushroom body of Apis. All parts
increase in volume as the insects get older. Foragers have bigger lips and collars in the calyces than nurse bees of the same age
and parents (after Durst et al., 1994).
556 NERVOUS SYSTEM
Axons from most of the retinula cells in the eye end in probable that, here, as in the lamina, the pattern of neural
the cartridges, although one or two from each ommatid- signals is a precise representation of any image falling on
ium pass through to the medulla (Fig. 20.21a). In flies, the the eye. This is called retinotopic mapping. Over 30
six retinula cells ending in the lamina have the same range neurons contribute to each column in the medulla. The
of spectral sensitivity with maximum sensitivity to green. axons of the ultraviolet-sensitive retinula cells, as well as
They form part of a color-insensitive (because they all axons of lamina neurons, terminate within these columns.
arise from cells with the same visual pigment) pathway In the lobula, some of the precision retained in the
which converges on to the giant interneurons in the lobula medulla is lost as the neural pathways converge, but the
(see below). The two cells extending to the medulla (shown convergence involves several different neural pathways
solid black in Fig. 20.21a) have different wavelength which run in parallel, each relaying information about par-
sensitivities and form part of a color-sensitive system con- ticular aspects of the visual field such as size, shape, move-
verging on the smaller interneurons of the lobula. ment and color. The most extensive studies are on
The cartridges of one insect are uniform in structure. In cyclorraphan flies, but similar principles probably apply to
the fly, 19 cells contribute to each one, and each group of other insects.
neurons is wrapped by a glial cell which effectively isolates Two types of interneuron are present in the lobula:
the cells within from extraneous inputs (Fig. 20.21a). The small-field neurons which receive inputs from a small
retinula cell axons that terminate in the lamina synapse with number of columns in the medulla, and wide-field neurons
monopolar interneurons whose axons run to the medulla receiving inputs from a very large number of columns (Fig.
and with other fibers having cell bodies in the medulla (cen- 20.21c). Small-field neurons in the fly receive inputs from
trifugal fibers). The monopolar cells are of two types: some about 12 to 150 columns representing a receptive field in
receive input only from retinula axons in a single cartridge, the eye that is 20 ° or less in diameter (Gilbert &
and they are known as small-field cells; others receive input Strausfeld, 1992; Strausfeld & Gilbert, 1992). Collectively,
from several cartridges, and are known as wide-field cells. these neurons receive inputs from the whole of the retina
The identity of each group of fibers from the cartridges so that a coarse-grained representation of the image is
is retained in a series of columns in the medulla and it is retained. They may be important in pattern recognition.
BRAIN 557
from ommatidia
a)
axon of retinula b)
small monopolar cell retinula cells
interneuron large monopolar
interneuron ommatidia
centrifugal axon
of interneuron
to medulla
c) soma of descending
small-field interneuron wide-field
neuron lobula plate neuron
from
medulla
from
medulla
synaptic connections
synaptic connections soma of with descending
with descending descending interneuron
interneuron interneuron
position of
esophagus
Fig. 20.21. Neurons of the optic lobe. (a) Diagram of an optic cartridge in the lamina of a fly. The side facing out of the page
has been cut away to show the arrangement of fibers within the cartridge (after Laughlin, 1975). (b) Relationship between a
cartridge in the lamina and the overlying ommatidia. In flies, which have an open rhabdom (see Fig. 22.3) the axons of retinula
cells with the same visual field (shown here in black) in adjacent ommatidia come together in one cartridge. In other insects,
each cartridge receives sensory axons only from the ommatidium immediately outside it. (c) Representation of wide-field and
narrow-field interneurons with arborizations in the lobula plate of a fly and their connections with descending interneurons
(based on Gronenberg & Strausfeld, 1992).
558 NERVOUS SYSTEM
In Sarcophaga, nine T-shaped wide-field neurons are (Figs. 20.16, 20.17). The latter is a relatively poorly
present in the lobula plate forming the so-called vertical defined region of neuropil containing the terminal arbor-
system, while three other cells with inputs from different izations of mechanosensory neurons from the scape and
parts of the eye form the ‘horizontal’ system (Fig. 20.21c). pedicel, and perhaps also from the flagellum of the
These cells receive inputs from large numbers of columns antenna. It also contains dendritic arborizations of the
in the medulla and their principal function is in detection motor neurons controlling the antennal muscles.
of different types of movement. The horizontal cells, for The antennal lobes are regions of neuropil, one in rela-
example, are excited by movement over the eye from front tion to each antenna, within which are discrete balls of
to back such as the insect would receive in normal forward dense synaptic neuropil which in some insects are sur-
movement, and are inhibited by movement from back to rounded by a layer of glial cells (Fig. 20.23a). These struc-
front (Fig. 20.22). They are thus well-suited to the percep- tures are called glomeruli. In the antennal lobe of Locusta
tion of yawing movements of the insect, but they do not there are about 1000 relatively poorly defined glomeruli,
respond to rolling movements because image movement is but Periplaneta has only 125 and Manduca about 64, while
vertical (Egelhauf, 1985; Hausen, 1982). Comparable Aedes has fewer than ten. Axons from olfactory sensilla on
wide-field neurons are present in other insects. the antenna terminate in the glomeruli, and each axon only
Both small- and wide-field interneurons have axons goes to one glomerulus (Christensen et al., 1995; Hansson
projecting to the deutocerebrum. Here they synapse with et al., 1992). Within a species, individual glomeruli appear
descending interneurons regulating the motor systems of to be constant in form and position. This is most obvious
the thorax that are involved in walking and flight (Fig. in the males of many Lepidoptera and of Periplaneta,
20.21c, and see Fig. 9.32). insects that are attracted to females by pheromones, where
Reviews: Kral, 1987 – lamina; Laughlin, 1981 – lamina; two or three larger glomeruli are grouped together
Strausfeld & Nässel, 1981 forming a macroglomerular complex to which the axons of
sex pheromone-specific neurons converge. The axons
20.4.2 Deutocerebrum from olfactory receptors on the maxillary and labial palps
The deutocerebrum contains the antennal (olfactory) also terminate in a glomerulus which, at least in Manduca,
lobes and the antennal mechanosensory and motor center does not receive inputs from the antennae.
BRAIN 559
soma soma
to
protocerebrum
glomerulus glomerulus
c)
central
mushroom body
body
soma
antennal lobe axon terminals in each
glomerulus
Within the antennal lobe, intrinsic (local) interneurons al., 1993). The physiological characteristics of the projec-
innervate several or even all of the glomeruli (Fig. 20.23b). tion neurons vary. Some respond only when the antennal
These local interneurons relay information to other inter- receptors are stimulated by a specific odor that is a regular
neurons, called projection neurons, connecting the olfac- feature in the life of the species, like a pheromone compo-
tory lobes to the mushroom bodies and other parts of the nent. A few may respond when the antenna is stimulated
protocerebrum (Figs. 20.18b, 20.23b). Some projection by specific mixtures of compounds that are of particular
neurons have uniglomerular arborizations; others are importance to the species, such as a pheromone blend
multiglomerular. It is common for the local interneurons (Christensen, Mustaparta & Hildebrand, 1995). Other
to inhibit activity in the projection neurons (Christensen et projection neurons, however, respond when the antenna is
560 NERVOUS SYSTEM
exposed to any one of a wide range of odors and it is proba- femur, interaction occurs between the sensory neurons
bly these neurons that provide the insect with general acting via an interneuron. The activity of one sensory axon
information about odors in the environment. activates the interneuron and causes it to inhibit activity in
Other interneurons provide input to the antennal other sensory axons. There are about 90 sensory axons
lobes. The serotonergic cell described above is of this type from the chordotonal organ and the effect of each one is
and its effect is presumably to modulate the transfer of regulated by the activity of the whole ensemble (Burrows
information within the glomeruli (Fig. 20.23c). & Matheson, 1994).
Reviews: Boeckh et al., 1990; Christensen & Hildebrand, 1987; Postsynaptic integration results from temporal and
Homberg, Christensen & Hildebrand, 1989 spatial summation.
femur, tibia and tarsus of the locust, Schistocerca, arborize stimulated and it is possible that the insect can also determine
in progressively more posterior and lateral regions of the which part of an antenna is stimulated. This is certainly the
neuropil in the relevant ganglion (Fig. 20.24a). Dorsal, case in male Periplaneta where some projection neurons from
ventral, medial and lateral positions of the hairs on the legs the macroglomerulus synapse with sensory axons from
also tend to be retained within the neuropil. Thus the different regions of the antenna (Hösl, 1990).
sensory neuropil contains a three dimensional representa- Many insects can distinguish between different odors
tion of the positions of the hairs on the legs. This is called a and this necessitates maintaining differences in the sensory
somatotopic map. Moreover, some of the spiking local input in the central nervous system. Sensilla sensitive to a
interneurons with which the sensory axons connect, retain specific odor appear to converge on a single glomerulus
the pattern from a single leg (Fig. 20.24b,c), but others independent of their position on the antenna. Thus the
incorporate information from other legs losing some of the array of glomeruli may contain an ‘odotopic’ map of the
spatial content of the signal so the map becomes much odor environment. (This is not to imply that the odors are
more coarse-grained. Some intersegmental interneurons spatially separated in the environment, but that the neural
also retain some of the positional information (Burrows, pathways responding to different odors are anatomically
1992; Burrows & Newland, 1993). separated). This is most evident in the case of male per-
This is more clearly seen in the cockroach escape ception of female sex attractant pheromones. Each part of
response. The trichoid sensilla on the cerci of the cock- the macroglomerular complex receives input from sensory
roach are differentially sensitive to deflection in different cells responding to one of the principal components of the
directions. Their axons connect with four giant inter- attractant pheromone, and all the units responding to that
neurons, two on each side, in a manner which retains the component terminate in the same part.
major components of directionality. Thus the inter- The extent of convergence of information from the
neurons are most responsive to deflection of the hairs olfactory sensilla to the olfactory glomeruli and sub-
backwards or forwards, to left or to right. This information sequently to the mushroom bodies is very great. For
is conveyed by the interneurons to the thorax where the example, in a male cockroach, Periplaneta, each antenna
output of motor neurons, producing a turn to left or right, carries about 195 000 olfactory neurons responding to
depends on the balance of activity between the inter- various environmental odors plus about 150 000 that
neurons on the two sides (Camhi, 1993). respond to components of the female pheromone. The
As the insect has contact chemoreceptors on the tarsi former converge on to 125 glomeruli, the latter to the
and other parts of the body, it is to be expected that posi- macroglomerular complex. About 280 output neurons leave
tional information is also necessary for the gustatory the olfactory lobe to convey information that forms the basis
system, in addition to quality coding. There is, at present, of behavioral responses. Similarly, the worker honeybee has
no information concerning differential distribution of the over 60 000 olfactory receptors on each antenna the axons of
arbors of gustatory cells within the ganglia, but, in general, which converge on to about 155 glomeruli.
gustatory sensilla contain a mechanosensitive neuron As each glomerulus is believed to receive sensory input
(section 24.2.1). As stimulation of the gustatory neurons from receptors for a specific compound, or perhaps class of
depends on contact with the substrate, the contact may be compounds, this system with its output neurons provides
sufficient to stimulate the mechanosensitive neuron and it ample basis for the discrimination of odors. The extent to
is possible that positional information about gustation is which odor discrimination is dependent on labelled lines
conveyed by these cells. It must also be inferred that some versus across-fiber patterning is not known. A labelled line
separation of taste quality, at least with respect to being responds only to a specific compound or combination of
acceptable or unacceptable, is maintained in the central compounds; such a system conveys information totally
nervous system, but there is no information on this. unambiguously. Across-fiber patterning requires the
Responses to olfactory stimuli also require processing of assessment of the overall input from an array of neurons
information about the source and the quality of the odor. with different ranges of sensitivity. The relatively large
Orientation with respect to an odor source is usually deter- numbers of glomeruli and output interneurons provide
mined mechanically from the direction of air movement. In the insect with the potential to distinguish a very large
addition, the right and left antennae may be differentially number of odors using across-fiber patterning.
562 NERVOUS SYSTEM
ventral
association
area
arborization of
spiking local
interneuron
receptive field of
interneuron
v d v
femur
tibia
tarsus
Fig. 20.24. Somatotopic mapping of mechanosensory input from the hind leg of a locust. All the mechanosensory axons from the
leg arborize in a ventral region of the neuropil known as the ventral association area (indicated by the dotted line). The diagrams at
the bottom represent the leg as if slit along the ventral side and flattened so that the dorsal midline is in the center, ventral midline
at the outer edges. Cross-hatching shows the area in which mechanical stimulation results in excitation of the interneuron shown
in the central panel (after Burrows & Newland, 1993). (a) Input from the femur. Top: the arborization of a mechanosensitive
neuron at the base of the femur. Center: the arborization of a spiking local interneuron which is excited by stimulation of the
ventral area of the femur, but not other parts of the leg (shown at bottom). (b) Input from the tibia. Top: the arborization of a
mechanosensitive neuron at the base of the tibia. Center: the arborization of a spiking local interneuron which is excited by
stimulation of the ventral area of the tibia, but not other parts of the leg (shown at bottom). (c) Input from the tarsus. Top: the
arborization of a mechanosensitive neuron on the basal tarsomere. Center: the arborization of a spiking local interneuron which is
excited by stimulation of the ventral area of the distal tarsus, but not other parts of the leg (shown at bottom).
CONTROLLING BEHAVIOR 563
period. The brain and subesophageal ganglion are necessary a) normal cycle
transcription
to develop long-term memory, but, once the information is RNA levels inhibited by
proteins in
acquired, the head is no longer essential, as the segmental nucleus
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21 Endocrine system
[570]
ENDOCRINE ORGANS 571
OH O
JH-I
ecdysone O
OH O
18 carbon atoms
HO O
OH JH-II
O
HO 7 O
17 carbon atoms
H
O
O
OH
JH-III
O
3-dehydroecdysone O
OH 16 carbon atoms
leucokinin Asp-Pro-Ala-Phe-Asn-Ser-Try-Gly-NH 2
ABBREVIATIONS
Fig. 21.3. Some of the major peptide hormones, with the amino acid sequences of some. Commonly used abbreviations are
given in brackets where appropriate. (a) Peptides involved in different stages of molting. (b) Peptides regulating juvenile
hormone synthesis. Note the similarities of the endings (shown in dotted rectangle) of the Diploptera allatostatins, and the
completely different structure of Manduca allatostatin. (c) Adipokinetic hormone and other hormones with similar
sequences. Dotted rectangles indicate similar positions of specific residues in at least four of the compounds shown. AKH,
adipokinetic hormone; HTH, hypertrehalosemic hormone. (d) Peptides involved in salt and water regulation. (e) Other
peptide hormones.
ENDOCRINE ORGANS 573
a) Cimex b) Hyalophora
corpus corpus
cardiacum allatum prothoracic spiracle
brain
brain
subesophageal
ganglion prothoracic
foregut prothoracic gland
gland
prothoracic
trachea ganglion
trachea
prothoracic spiracle
salivary ducts
salivary
gland
Fig. 21.4. Prothoracic glands shown by dark shading. General arrangement: (a) in larval bed bug, Cimex (after Wells, 1954);
(b) in pupal silk moth, Hyalophora (after Herman & Gilbert, 1966).
21.2.1 Endocrine glands in the larva of Diatraea to almost 250 in Hyalophora. The
21.2.1.1 Glands producing ecdysteroids cells in these species do not divide, but undergo endo-
In the immature stages of all insects, molting hormones mitotic division so that they become polyploid, increasing
are produced by the prothoracic glands. In adult females, greatly in size through larval life. The glands show cycles
where the same hormones are produced to regulate of development associated with secretion.
embryonic development, the follicle cells in the ovary are The prothoracic glands degenerate in the adults of
the principal source, although there is evidence that some nearly all insects, but they persist in Apterygota, which
ecdysteroids are produced elsewhere in the abdomen of continue to molt throughout life, and in the adults of
some insects, possibly by the oenocytes. solitarious locusts. Normal persistence of the glands
throughout development results from the presence of
Prothoracic glands The prothoracic, or thoracic, glands are juvenile hormone in the hemolymph; their breakdown
a pair of usually diffuse glands at the back of the head or in after adult emergence is due to the lack of this hormone.
the thorax in most insects (Fig. 21.4), but in the base of the
labium in Thysanura. Each gland has a rich tracheal supply 21.2.1.2 Corpora allata
and often a nerve supply. In most insects, the nervous The corpora allata are glandular bodies, usually one on
connection is with the subesophageal ganglion, but in some either side of the esophagus (see Fig. 20.16) although they
there is also a connection to the prothoracic ganglion, and, may be fused to form a single median organ as in higher
in cockroaches, there is a connection to the brain. The pro- Diptera. Each is connected with the corpus cardiacum on
thoracic glands of Heteroptera have no nerve supply. the same side by a nerve carrying fibers from neuro-
The glandular cells making up the gland in most hemi- secretory cells of the brain. In addition, a fine nerve con-
metabolous insects and in Coleoptera are small, up to nects each corpus allatum with the subesophageal
25 m across, and they are present in large numbers and ganglion. This is a major nerve in Ephemeroptera, where
undergo cycles of mitosis. In larval Tenebrio, there are up the nerve from the corpus cardiacum is absent. In
to 1000 cells. However, in most other holometabolous Thysanura, the corpora allata are in the bases of the maxil-
insects and in Heteroptera, the cells are large, and they are lae and, in addition to a fine nerve direct from the sub-
present in relatively small numbers, ranging from about 30 esophageal ganglion, they are innervated by branches from
574 ENDOCRINE SYSTEM
anterior posterior Fig. 21.6) and they appear to release their contents during
midgut midgut
the six hours after a meal (Brown, Crim & Lea, 1986). It is
possible that these cells are involved in the regulation of
enzyme synthesis and release.
RFamide
Other cells may have different functions, perhaps
including the regulation of gut motility. The midgut epi-
thelia of several caterpillars have been shown to contain
urotensin peptides that induce contractions in visceral muscles (Yi,
Tirry & Degheele, 1992).
The areas at which secretions of neurosecretory cells leave the ganglion in the median interganglionic connec-
are released into the hemolymph are called neurohemal tive and diverge laterally forming swollen structures called
areas, or, if a well-defined structure is formed, neurohemal perivisceral or perisympathetic organs; others may reach
organs. The corpora cardiaca are the neurohemal organs at the same structures via the lateral nerves. In some cases,
which many of the hormones produced in the brain enter the neurohemal areas occur along the lateral nerves
the hemolymph (see below). without the development of discrete neurohemal organs.
The somata of neurosecretory cells occur in all the Some neurosecretory cell bodies occur outside the
ganglia of the central nervous system. Examples of a few of central nervous system. In Carausius there are 22 neuro-
the cells in the ganglia of the caterpillar of Manduca for secretory cells with somata on the peripheral nerves in
which the nature of their secretion is known are given in each abdominal segment. Unlike the neurosecretory cells
Fig. 21.7. in the central nervous system, they are multipolar cells.
In the brain, there are often two main groups of neuro- Others, called cardiac cells, are present alongside the heart.
secretory cells on each side. One group is in the pars inter- It is uncertain if these cells are connected to the central
cerebralis, near the midline. The number of apparent nervous system.
neurosecretory cells in this group is very different in The secretions of neurosecretory cells are usually
different species. The desert locust, Schistocerca, for neuropeptides, but in some cases they are known to be bio-
example has about 500, whereas Aphis has only four or genic amines. The products are synthesized in the soma
five. The axons from these cells pass backwards through where they are associated with a protein to form mem-
the brain and some or all of them cross over to the opposite brane-bound granules. It is these granules which are
side (decussate), emerging from the brain as a nerve which visualized in studies on neurosecretion. The granules are
runs back to the corpus cardiacum. Most of the fibers end transported along the axon to the terminals at rates
here, but a few pass through the corpus cardiacum to the varying from 5 to 21 mm h⫺1 and released from the termi-
corpus allatum and, in the locust, to the foregut and inglu- nals by exocytosis. Exocytosis results in a temporary
vial ganglion. In most Apterygota, these median neuro- increase in the surface membrane of the axon as the mem-
secretory cells are contained in separate capsules of brane around the granules fuses with the plasma mem-
connective tissue, known as the lateral frontal organs, on brane. Membrane is subsequently retrieved by
the dorsal side of the brain, but in some Machilidae the micropinocytosis and the small size of the vesicles, about
cells are intercerebral as in Pterygota. Petrobius, also a 40 nm diameter, ensures that only a minimum amount of
machilid, occupies an intermediate position with some extracellular fluid is taken up for a relatively large retrieval
neurosecretory cells in the lateral frontal organs and of membrane. Presumably the small vesicles are broken
others in an adjacent frontal zone of the brain (Watson, down and the material re-cycled.
1963). Neurosecretory cells resemble normal neurons in
The second group of neurosecretory cells in the brain having an excitable plasma membrane. They conduct
is variable in position. It is sometimes medial to the action potentials, and this electrical activity leads to release
corpora pedunculata, and sometimes between the latter of the neurosecretory material at the axon terminals just as
and the optic lobes. In some Diptera and Hymenoptera, an action potential in a normal neuron causes the release of
the cells corresponding with this group are associated with neurotransmitter at a synapse. The axon potentials are
the other neurosecretory cells in the pars intercerebralis. A generally much longer lasting than those in other neurons,
second axon tract passes from these cells through the brain however, with durations up to 20 ms. The secretory activ-
to the corpus cardiacum and, in Schistocerca, some fibers ity of a neurosecretory cell is regulated by neurons making
also extend to the corpus allatum. synaptic connections with its dendritic arbor. The inputs
Variable numbers of neurosecretory cells occur in the to the cell may be excitatory or inhibitory.
ventral ganglia. Their products are released into the hemo- The endocrine activity of neurosecretory cells may take
lymph at various neurohemal sites. For example, the axons one of two forms: the cells may either produce hormones
of cells in the subesophageal ganglion of Manduca run to which act directly on effector organs or they may act on
the corpora cardiaca via the brain or the lateral nerves (Fig. other endocrine organs, which, in turn, are stimulated to
21.7). The axons of some cells in the abdominal ganglia produce hormones. Adipokinetic hormone is an example
ENDOCRINE ORGANS 577
a)
maxillary
nerve
PTTH brain
b)
eclosion subesophageal
BRAIN hormone ganglion
corpus
cardiacum
corpus
allatum
circumesophageal
connective
mandibular
neuromere
proctolin-like maxillary
SUBESOPHAGEAL neuromere
GANGLION PBAN-like
labial
neuromere
interganglionic
connective
perivisceral hindgut
organ
CCAP-like
ABDOMINAL
GANGLION
PBAN-like
median
nerve
to to perivisceral
hindgut organ via
transverse segmental
nerve nerve
Fig. 21.7. Examples of neurosecretory cells and neurohemal organs in the larva of Manduca. (a) Connections of some
neurosecretory cells with their neurohemal organs. Bold arrows indicate release of peptides into hemolymph. Only a few of the
cells are shown. Note that, in most insects, the corpora cardiaca are the neurohemal organs for prothoracicotropic hormone
(PTTH); the Lepidoptera are unusual in using the corpora allata for this purpose. It is important to note that the suffix ‘like’ on
some labels indicates that the peptides in the labelled cell are similar to, but not necessarily the same as the named peptide.
Their functions are generally unknown. Abbreviations: CCAP, crustacean cardioactive peptide; PBAN, pheromone
biosynthesis activating neuropeptide (based largely on data of Dr. N.T.Davis). (b) Eclosion hormone is released from
neurohemal areas on the hindgut. The position of the soma in the brain is shown in (a) (after Truman & Copenhaver, 1989).
578 ENDOCRINE SYSTEM
ecdysteroids
regulating corpus allatum activity, allatotropins and allato- juvenile ecdysteroids
hormone PTTH
JH +
statins, are examples of peptides regulating the synthesis
of other hormones.
The contents of some neurosecretory cells react with
JH in
antisera of more than one neuropeptide and it is likely that hemolymph
these cells secrete cocktails of peptides each producing a
ecdysteroid in
hemolymph
different, though probably related, effect (Homberg, Davis
& Hildebrand, 1991).
Reviews: Orchard & Loughton, 1985; Raabe, 1975, 1983
JH titer (µM)
JH synthesis (pmol.h -1)
synthesis
75 target
corpus tissues
cardiacum
50 5
titer
corpus juvenile
25 allatum hormone
JH esterase
and
epoxide hydrolase
0 0
0.6 1 1.4
Malpighian
oocyte length (mm) tubule JH metabolites
excreted
b) Manduca
25
Fig. 21.11. Juvenile hormone. Regulation of hemolymph titer
20 JH esterase involves the balance between synthesis in the corpora allata and
(nmol.min -1.ml-1)
esterase activity
a) ecdysteroids protein
kinase
larva 5 pupa
adenylate inactive
hemolymph titer
cyclase
ATP cAMP
G protein
active
PTTH
++ protein
Ca
PTTH synthesis
receptor
ecdysone
synthesis
cell wall
b) receptors on epidermal cells
endoplasmic
reticulum ecdysone
abundance
hormones and the pheromone biosynthesis activating only initiates ecdysone formation in the prothoracic
neuropeptide (PBAN) act via cAMP, but the activation of gland, but also promotes the production of -tubulin
glycogen phosphorylase by adipokinetic hormone appears which may be important in the transport of ecdysteroid
to involve a different pathway. Eclosion hormone triggers precursors within the cells (Rybczynski & Gilbert, 1995).
ecdysis behavior via an increase in cGMP accompanied by In the epidermis, ecdysone initiates the de novo synthesis
an increase in inositol trisphosphate although the exact of DOPA decarboxylase and also activates the enzyme
relationship between these two messengers is unclear which catalyses the synthesis of a phenol oxidase from its
(Morton & Simpson, 1995; Smith & Sedlmeier, 1990; proenzyme, making available the essential enzymes for
Spring, 1990). cuticular tanning.
A hormone may lead to the production or activation Reviews: Riddiford, 1994 – juvenile hormone; Riddiford, 1995 –
of not just one, but a suite of enzymes necessary to Lepidoptera; Riddiford & Truman, 1993 – ecdysteroids;
produce and ensure the successful secretion of the final Truman, 1995 – Lepidoptera; Wyatt & Davey, 1996 – juvenile
product. For example, prothoracicotropic hormone not hormone in adult insects
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Sesma, P., López, J. & Vázquez, J.J. Model Systems in the Lepidoptera, ed. Sparagana, S.P., Bhaskaran, G. & Barrera,
(1989). Ultrastructure and M.R. Goldsmith & A.S. Wilkins, pp. P. (1985). Juvenile hormone acid
immunocytochemistry of endocrine 293–322. Cambridge: Cambridge methyltransferase activity in imaginal
cells in the midgut of the desert University Press. discs of Manduca sexta prepupae.
locust, Schistocerca gregaria (Forskal). Riddiford, L.M. & Truman, J.W. (1993). Archives of Insect Biochemistry and
Cell and Tissue Research, 258, Hormone receptors and the regulation Physiology, 2, 191–202.
577–83. of insect metamorphosis. American Spring, J.H. (1990). Endocrine regulation
Zoologist, 33, 340–7. of diuresis in insects. Journal of Insect
Physiology, 36, 13–22.
584 ENDOCRINE SYSTEM
Stay, B., Sereg Bachmann, J.A., Truman, J.W. (1995). Lepidoptera as Yamashita, O. (1996). Diapause hormone
Stoltzman, C.A., Fairbairn, S.E., Yu, model systems for studies of hormone of the silkworm, Bombyx mori: struc-
C.G. & Tobe, S.S. (1994). Factors action in the central nervous system. In ture, gene expression and function.
affecting allatostatin release in a cock- Molecular Model Systems in the Journal of Insect Physiology, 42,
roach (Diploptera punctata): nerve Lepidoptera, ed. M.R. Goldsmith & 669–79.
section, juvenile hormone analog and A.S. Wilkins, pp. 323–39. Cambridge: Yi, S.-X., Tirry, L. & Degheele, D. (1992).
ovary. Journal of Insect Physiology, 40, Cambridge University Press. Presence of myotropins in larval
365–72. Truman, J.W. & Copenhaver, P.F. (1989). midgut extracts of lepidopteran insects:
Stay, B., Tobe, S.S. & Bendena, W.G. The larval eclosion hormone neurons Manduca sexta, Agrotis segetum and
(1994). Allatostatins: identification, in Manduca sexta: identification of the Spodoptera exempta. Journal of Insect
primary structures, functions and dis- brain-proctodeal neurosecretory Physiology, 38, 1023–32.
tribution. Advances in Insect Physiology, system. Journal of Experimental Yin, C.-H., Zou, B.X., Jiang, M., Li, M.-
25, 267–337. Biology, 147, 457–70. F., Qin, W., Potter, T.L. & Stoffolano,
Stay, B. & Woodhead, A.P. (1993). Veenstra, J.A., Lau, G.W., Agricola, H.-J. J.G. (1995). Identification of juvenile
Neuropeptide regulators of insect & Petzel, D.H. (1995). hormone III bisepoxide (JHB3), juve-
corpora allata. American Zoologist, 33, Immunohistological localization of nile hormone III and methyl farnesoate
357–64. regulatory peptides in the midgut of secreted by the corpus allatum of
Tobe, S.S. & Stay, B. (1985). Structure the female mosquito Aedes aegypti. Phormia regina (Meigen), in vitro and
and regulation of the corpus allatum. Histochemistry and Cell Biology, 104, function of JHB3 either applied alone
Advances in Insect Physiology, 18, 337–47. or as a part of a juvenoid blend. Journal
305–432. Watson, J.A.L. (1963). The cephalic of Insect Physiology, 41, 473–9.
Touhara, K., Bonning, B.C., Hammock, endocrine system in the Thysanura. Žitňan, D., Kingan, T.G., Hermesman,
B.D. & Prestwich, G.D. (1995). Action Journal of Morphology, 113, 359–73. J.L. & Adams, M.E. (1996).
of juvenile hormone (JH) esterase on Wells, M.J. (1954). The thoracic glands of Identification of ecdysis-triggering
the JH–JH binding protein complex. Hemiptera Heteroptera. Quarterly hormone from an epitracheal endocrine
An in vitro model of JH metabolism in a Journal of Microscopical Science, 95, system. Science, 271, 88–91.
caterpillar. Insect Biochemistry and 231–44. Žitňan, D., Sauman, I. & Sehnal. F.
Molecular Biology, 25, 727–34. Wyatt, G.R. & Davey, K.G. (1996). (1993). Peptidergic innervation and
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Biochemistry and Physiology 103B, Insect Physiology, 26, 1–155.
795–807.
PART V
Communication
a) a)
corneal lens b)
corneal lens
nucleus of
crystalline Semper cell
cone
rhabdom
crystalline
cone
primary pigment
basal lamina cell
axons
c)
rhabdom
retinula cell
secondary pigment
d) cell
microvilli - collectively
forming the rhabdom
basal lamina
axon
retinula
cells
1 µm
Fig. 22.1. Apposition eye: (a) diagrammatic section through an apposition eye showing the rhabdoms extending to the
crystalline cones.; (b) ommatidium; (c) surface view of part of an eye showing the outer surfaces of some corneal lenses
(facets); (d) cross-section through a fused rhabdom (Apis) (after Goldsmith, 1962).
rhabdom (although the cells are not actually fused), but Camponotus, and, in Drosophila, with an open rhabdom,
Diptera, Dermaptera, some Heteroptera and some each rhabdomere is 60 m long. It is usually shorter in
Coleoptera have widely separated rhabdomeres forming superposition eyes, and even in apposition eyes one of the
an ‘open’ rhabdom (Fig. 22.3). In a fused rhabdom, all the rhabdomeres may be very short (see Fig. 22.5a, cell 9).
retinula cells within one ommatidium have the same field There is much variation in the way that the clear zone
of view. In species with open rhabdoms each retinula cell in superposition eyes is bridged. In many Lepidoptera and
within an ommatidium has a separate visual field, shared Coleoptera, the retinula cells extend to the crystalline cone
by individual cells in each of the adjacent ommatidia (see as a broad column, but the rhabdom is restricted to the
Fig. 20.21b). basal region (Fig. 22.2c), but, in Carabidae and Dytiscidae,
The rhabdom of apposition eyes usually extends the one of the retinula cells also has a short distal rhabdomere
full length of the retinula cells between the crystalline cone just below the cone. In other Lepidoptera (the
and the basal lamina. It is 150 m long in the ant, Bombycoidea and Hesperioidea), the retinula cells of each
COMPOUND EYES 589
a)
corneal lens
b) Photuris
DARK LIGHT
crystalline ADAPTED ADAPTED
cone
corneal
lens
clear zone
rhabdom pigment
basal lamina cells
axons Semper
cell
c) Archichauliodes crystalline
tract
clear
DARK LIGHT zone
ADAPTED ADAPTED
corneal
lens pigment
cells
crystalline
cone retinula
cell
primary
pigment rhabdomere
cell
clear secondary basal
zone pigment cell lamina
retinula axons
cells
rhabdom
basal
lamina
axons
Fig. 22.2. Superposition eye. (a) Diagrammatic section through a superposition eye showing the clear zone between the
rhabdoms and the lens systems. (b) Exocone eye in which the clear zone is crossed by a crystalline tract formed from the
Semper cells. Note that there is no crystalline cone in exocone eyes. Left: dark-adapted; right: light-adapted (Photuris,
Coleoptera). (c) Eucone eye in which the clear zone is bridged by retinula cells. Left: dark-adapted; right: light-adapted
(Archichauliodes, Megaloptera) (after Walcott, 1975).
ommatidium form a thin strand, which may be only 5 m tracheae form a layer at the back of the eye. This layer
across, to the lens. This strand is called a crystalline tract. which reflects light back into the eye is called a tapetum.
Beetles with exocone eyes (see below) have a similar struc- The taenidia of the tracheae forming the tapetum are
ture, but it is formed by the Semper cells and the retinula flattened and enlarged. Their cuticle consists of many suc-
cells are restricted to a basal position in the ommatidium cessive layers each about one quarter of the wavelength of
(Fig. 22.2b). light in thickness with alternate layers having high and low
The sensory parts of each ommatidium are usually sur- refractive indices. Light is reflected at each boundary, pro-
rounded by 12–18 secondary pigment cells so that each ducing interference colors (section 25.2.2). In butterflies,
ommatidium is isolated from its neighbors. the reflected light from the back of the eye doubles the
Tracheae pass between the ommatidia proximally in effective length of each rhabdom as the light passes
some species, and, in many Lepidoptera, closely packed through it twice. In moths, with superposition eyes, the
590 VISION
50
d) facet f)
diameter small facet
diameter
smaller radius
3o { of curvature
interommatidial
angle
e) interommatidial 1o {
angle
large facet
diameter maximum radius
optical of curvature
axis
the Semper cells. It is usually conical, but in some groups, Diptera and in Heteroptera. In Elateridae and
notably in Collembola and Thysanura, it is more or less Lampyridae, the Semper cells do not contribute to the
spherical. In a few beetles, some Odonata and most lens. Instead, the corneal lens forms a long cone-shaped
Diptera the Semper cells secrete an extracellular cone projection on the inside (Fig. 22.2b). This is known as the
which is liquid-filled or gelatinous rather than crystalline. exocone condition.
Ommatidia with this type of lens are called pseudocone
ommatidia. The Semper cells do not produce a separate Variation in the retinula cells Although it is common for
lens in some species, but their cytoplasm is clear and they all the retinula cells to be of similar length and to form a
occupy the position of the cone. These acone eyes are rhabdomere all along the inner margin, this is not always
present in various families of Coleoptera, for example true. The ommatidia of Apis have nine retinula cells. Eight
Coccinellidae, Staphylinidae and Tenebrionidae, in some of them have more or less similar rhabdomeres distally, but
592 VISION
Fig. 22.5. Different rhabdoms, showing a longitudinal section of an ommatidium with transverse sections at the positions
shown. Numbering of retinula cells is for clarity; the numbers have no other significance. (a) Twisted rhabdom. The retinula
cells twist through 180° from top to bottom of the rhabdom. Each retinula cell is given the same number in cross-sections at
different levels in the eye. Twisting is not shown in the longitudinal section, but note the short ninth cell which only
contributes to the rhabdom proximally (Apis). (b) Tiered rhabdom. Four retinula cells contribute to the more distal rhabdom,
three others to the proximal rhabdom (Lepisma, Thysanura) (after Paulus, 1975). (c) Tiered rhabdom in a superposition eye.
Only the proximal part of the eye is shown. Cell 8 only contributes to the rhabdom proximally; distally, cell 1 contributes a
major proportion (Spodoptera, Lepidoptera) (after Langer, Hamann & Meinecke, 1979).
proximally, two cells (cells 1 and 5 in Fig. 22.5a) do not functions as an independent unit. Each lens produces a
contribute to the rhabdom while the rhabdomere of the small inverted image of the object in its field of view which
short, ninth cell is present. Many other insects have ret- is in focus at the tip of the rhabdom (Fig. 22.6a). Because
inula cells of different lengths so that they have a tiered the retinula cells in most ommatidia are twisted, they all
arrangement, as in Lepisma (Fig. 22.5b), or as in receive the same signal, and the image formed by the lens is
Spodoptera (Fig. 22.5c). Many other arrangements are not preserved. The light reaching the rhabdom in each
known. ommatidium has an overall intensity which varies from one
ommatidium to the next depending on the amount of light
reflected by the object in the field of view, and collectively
22.2 FUNCTIONING OF THE EYE the rhabdoms receive a mosaic of spots of light of different
intensities, which form an image of the object.
22.2.1 Image formation By bringing the light to a focus at the tip of the
Image formation depends on the optical properties of the rhabdom, the insect maximizes the amount of light
corneal lens and the crystalline cone. Refraction of light entering the rhabdom. In flies, with neural superposition
occurs at any interface with a difference in refractive index eyes, the amount of light available from each point in
on the two sides. In most apposition eyes, the outer surface space enters through seven ommatidia (see Fig. 20.21b)
of the corneal lens is the principal or only refracting so the signal contains more photons than light entering
surface, although, in butterflies, further refraction occurs through a single lens. Consequently, flies have greater
in the crystalline cone. sensitivity at low light intensities than insects with fused
In an apposition eye, each ommatidium is separated rhabdoms.
from adjacent ommatidia by screening pigment, so each Dark-adapted superposition eyes function in a very
FUNCTIONING OF THE EYE 593
inverted
lens image
refraction at
air-lens inverted
interface lens image
object
object
internal refraction due
to differences in
refractive index
internal
refraction
in lens
lenses lenses
image
rhabdoms clear zone
image
rhabdoms
Fig. 22.6. Image formation: (a) in an apposition eye, each lens forms an inverted image at the tip of the rhabdom (above), but
because the rhabdomeres function as a single unit the impression of this image is not retained. Consequently the output from
each rhabdom is a response to the overall intensity of light that reaches it. Information concerning the object is thus
represented as a series of spots differing in intensity (below; suggested by the dotted arrow); (b) in a superposition eye, light
rays are refracted internally within the lens (above). They are unfocused as they exit the lens, but collectively form a single
upright image at the tips of the rhabdoms (below).
1.49 1.47 1.46 1.45 1.54 1.52 1.49 1.46 1.45 1.44 it causes a structural change producing, in a series of steps,
metarhodopsin. This form of metarhodopsin activates G
proteins with high efficiency and so initiates a second mes-
senger cascade leading to an amplification of the energy of
1.0 1.36
the reaction and, ultimately, to a change in the membrane
potential of the retinula cell (Fig. 22.8b).
The metarhodopsin quickly loses its efficiency in acti-
corneal crystalline clear
air vating G proteins as a result of phosphorylation and
lens cone zone
binding to a protein, probably arrestin. The metarhodopsin
Fig. 22.7. Lens cylinder from a superposition eye. The refractive is, itself, photosensitive, absorbing light at a different wave-
index changes within the corneal lens and crystalline cone so that length from the rhodopsin giving rise to it. Photoactivation
refraction occurs within the lenses as well as at the air/corneal reconverts the metarhodopsin to inactive rhodopsin which,
lens and crystalline cone/clear zone interfaces (after Horridge, after dephosphorylation and release from arrestin, is avail-
1975).
able to transduce light again. Thus light of a different wave-
length from that to which the photopigment is sensitive
decreased when the eye becomes dark-adapted and light may contribute to the efficiency of the response and, under
from a greater area is admitted to each unit (see below). constant light conditions, the amounts of rhodopsin and
Diffraction within the eye results in light loss and, with metarhodopsin are in equilibrium. Different visual pig-
very small diameter lenses, this becomes critical. High ments produce metarhodopsins with different absorption
resolution requires large diameter facets, and this is spectra (Kiselev & Subramaniam, 1994; Stavenga, 1992).
achieved in some insects by a large radius of curvature of a The probability that a photon will encounter a visual
part of the eye. In this way it is possible to maximize the pigment molecule is increased by the length of the rhab-
lens aperture and retain small interommatidial angles. domere and by the rhabdom acting as a lightguide or a
Robber flies, Asilidae, and mantids have an area at the front waveguide (Fig. 22.9). In a light guide, light passes along
of the eye where the facets are larger and the inter- its length as a result of reflection at the boundaries of the
ommatidial angles are smaller than elsewhere (Fig. 22.4). rhabdom with the cytoplasm of the retinula cells. Light
This gives them a high level of resolution in the part of the entering the rhabdom within about 10 ° of its long axis (the
eye involved in prey detection and fixation. By analogy angle varies with the diameter of the rhabdom) is totally
with vertebrate eyes, the zone of highest resolution is reflected and so contained within the rhabdom, but some
sometimes called the fovea or acute zone. Many male of the light entering at more oblique angles is lost.
Diptera also have a forwardly directed acute zone which is However, if the rhabdom, or the separate rhabdomeres in
presumed to be important in following the rapid move- insects with an open rhabdom, is 0.5 m or less in diame-
ments of females during mating flights. Other male ter, approaching the wavelength of light, it functions as a
insects, like bibionids and mayflies, have upwardly waveguide. This differs from a lightguide because the light
directed acute zones in the eyes. These species form male waves interfere with each other producing a series of
swarms and perhaps use the eyes to detect females which modes in which the light is not uniformly distributed
fly into the swarm. across the rhabdom. These modes form stable patterns
Reviews: Land, 1985, 1989, 1997; Warrant & McIntyre, 1993 which travel along the rhabdom either within or outside it.
Because of these properties, light entering the
22.2.3 Transduction rhabdom tends to be retained within it and a high propor-
The conversion of light to electrical energy involves the tion is absorbed by the visual pigment. A tapetum, when
visual pigment. This is a chromoprotein belonging to a present, reflects light back into the eye and so further
group of chromoproteins known as rhodopsins. It consists increases the chances that the photons and receptor mole-
of retinal, the aldehyde of vitamin A, conjugated with a cules will interact.
protein (opsin) (Fig. 22.8a). It is a transmembrane protein Because the energy is amplified by a second messenger
in the microtubules forming the rhabdomeres. The 11-cis cascade, the interaction between a single photon and a
isomer of retinal is unstable and a photon interacting with receptor molecule is sufficient to produce a transient
FUNCTIONING OF THE EYE 595
a) b)
CH 3 CH 3 CH 3 CH 3 light
CH 2 OH (480 nm)
dephosphorylation in rhodopsin
vitamin A dark (active)
and
CH 3 release from arrestin [cis-retinal]
rhodopsin
rhodopsin [trans-retinal]
CH 3 CH 3 CH 3 CH 3 (inactive) G protein
CHO (inactive)
light
trans - retinal
(580 nm)
CH 3
metarhodopsin metarhodopsin
(low efficiency) (high efficiency)
CH 3 CH 3 CH 3
depolarization
retinal + opsin (protein) = rhodopsin
Fig. 22.8. Signal transduction: changing the energy of light to electrical energy. (a) Vitamin A and retinal. 11-cis-retinal is
unstable and is reconverted to trans-retinal by the energy of light. (b) The pathway by which light at one wavelength leads to
depolarization and then, at a different wavelength, to the regeneration of rhodopsin. The wavelengths shown are the
absorption maxima for a blue-sensitive rhodopsin (480 nm) and the metarhodopsin (580 nm) to which it is transformed. In the
active rhodopsin molecule, retinal is in the unstable cis form. Light with a wavelength of 480 nm produces isomerization to the
trans form, and, in a series of steps, this is converted to a form of metarhodopsin which activates G proteins with high
efficiency and leads to depolarization of the cell membrane. The metarhodopsin is unstable and is mostly transformed to a
form with low efficiency for activating G proteins, but some decays to retinal and opsin, especially at high light intensities.
Rhodopsin is regenerated, in an inactive form, from metarhodopsin by light of 580 nm wavelength. Active rhodopsin is slowly
produced from the inactive form in the dark. Rhodopsins with different absorption maxima produce metarhodopsins
absorbing maximally in different ranges from that shown (based on Kiselev & Subramaniam, 1994).
change, called a ‘bump’, in the membrane potential, often polarization of the interneuron. Any new signal is
large enough to lead to a response in the postsynaptic cells of amplified at these synapses while the effects of the general
the lamina. The size of the receptor potential increases with level of illumination are reduced. The mechanisms pro-
the intensity of illumination as more photons interact with ducing these effects are not fully understood, but involve
molecules of visual pigment, but the relationship between presynaptic interactions (Laughlin & Osorio, 1989).
intensity and response is not linear and above a certain level,
further increases in light intensity have no further effect on 22.2.4 Adaptation
the receptor potential, which is said to be saturated. For any The natural change from darkness to full sunlight involves
one insect, receptor potential increases with intensity over a a change in light intensity of some 10 log units: a white
range of about four orders of magnitude (Fig. 22.10). Below surface in bright sunlight reflects about 4 ⫻1020
this range, the cells do not respond; above it, their output is photons m⫺2 sr⫺1 s⫺1 compared with about 1010
maximal and shows no further increase. photons m⫺2 sr⫺1 s⫺1 on an overcast night with no moon,
Action potentials are not produced by retinula cells and and 1014 photons m⫺2 sr⫺1 s⫺1 on a moonlit night.
depolarization is transmitted along their axons by passive However, the response of the retinula cells is fully satu-
conduction. In the lamina, most of the retinula cells rated by an increase in intensity of about four log units
synapse with large monopolar cells, and with other inter- (Fig. 22.10). Various devices are used to regulate the
neurons (see Fig. 20.21c). The neurotransmitter at these amount of light reaching the receptors so that the insect
synapses is histamine and the signal is inverted. That is, a can operate over a wider range of intensities. The eye is
depolarization of the retinula cell produces a hyper- said to adapt to the light conditions.
596 VISION
n lower intensities
dynamic range of dark-
higher intensities
produce no saturate the
adapted eye
response response
1
relative response
dark-
adapted
0.5
light-
partial adapted
reflection
-4 -2 0 2 4 6
rhabdom relative light intensity (log scale)
light-adapted
dark-adapted
endoplasmic
reticulum
b) dark-adapted
retinula
cells
pigment
granule
rhabdom
palisade
FUNCTIONING OF THE EYE 599
pigment absorbing maximally at 568 nm; this pigment is When light is polarized, all wavelengths are affected,
absent from the dorsal ommatidia of males (Bernard & but the polarization receptors of ants and bees are respon-
Remington, 1991). sive to ultraviolet light. In Cataglyphis, six of the eight ret-
Sometimes retinula cells with different pigments are inula cells in the dorsal rim ommatidia are
anatomically differentiated. For example, in Apis the short ultraviolet-sensitive; four have a common orientation of
basal cell is one of the ultraviolet-sensitive cells, and in their microvilli, those of the other two are at right angles
Spodoptera the basal cell (cell 8) is red-sensitive and the (Fig. 22.15a). Consequently, when one set of cells is
distal cell (cell 1) ultraviolet- or blue-sensitive (Fig. 22.5c). responding maximally because its microvilli are parallel
Reviews: Peitsch et al., 1992; White, 1985 with the plane of polarization, the other set is responding
minimally. Each ommatidium in the dorsal rim responds
22.2.6 Discrimination of the plane of vibration maximally to polarization in one plane, and the population
(polarization sensitivity) of receptors exhibits a range of different orientations (Fig.
Light waves vibrate in planes at right angles to the direc- 22.15b). In the medulla of the optic lobe, the retinula cell
tion in which they are travelling. These planes of vibration axons synapse with interneurons responding maximally to
may be equally distributed through 360 º about the direc- polarization in a particular plane (Fig. 22.15c) (Labhart,
tion of travel, or a higher proportion of the vibrations may 1996). It is believed that, by scanning the sky, the insect is
occur in a particular plane. Such light is said to be polar- able to match the inputs of its polarization receptors to the
ized, and if all the vibrations are in one plane the light is pattern in the sky. When reorienting it matches the sky
plane-polarized. pattern to the remembered neural input.
Light coming from a blue sky is polarized. The degree Review: Wehner, 1989
of polarization and the plane of maximum polarization
from different parts of the sky varies with the position of 22.2.7 Magnetic sensitivity
the sun (Wehner, 1989). It is, consequently, possible to A number of insect species have been shown to respond to
determine the position of the sun, even when it is changes in magnetic field and it is possible that they use the
obscured, from the composition of polarized light from a earth’s magnetic field in navigation (Schmitt & Esch,
patch of blue sky. Certain insects are able to make use of 1993; Towne & Gould, 1985). Two mechanisms have been
this information in navigation. It is particularly important proposed to account for this response. Some insects are
in the homing of social Hymenoptera, and is best known in known to contain particles of magnetite, an iron oxide,
Apis and the ant, Cataglyphis. In other insects, including which might be affected by the magnetic field. In worker
Odonata and some Diptera, the ability to perceive polar- honeybees, the magnetite is contained in a ring of inner-
ized light probably enables the insects to maintain a con- vated oenocytes in each abdominal segment (Hsu & Li,
stant and steady orientation. 1994). Alternatively, it is possible that the compound eyes
Detection of the plane of polarization is possible are involved, and that magnetism affects electron spin res-
because photopigment molecules are preferentially ori- onance in one of the photoreceptors. In keeping with this
ented along the microvilli of the rhabdomere and possibility, the orientation of male Drosophila in a magnetic
maximum absorption occurs when light is vibrating in the field is affected by the wavelength of light in which they are
same plane as the dipole axis of the pigment molecule. If tested. In ultraviolet light (wavelength 365 nm) they exhib-
the rhabdom is twisted, as in most ommatidia, there can be ited a consistent magnetic compass orientation towards a
no preferred plane of absorption; polarization sensitivity direction to which they had been trained. Tested in
depends on a uniform orientation of the visual pigment blue–green light (500 nm), they oriented at right angles to
molecules within a rhabdomere. In ants and bees, and the training angle (Phillips & Sayeed, 1993).
other insects responding to the plane of polarization,
straight rhabdomeres are present only in a small group of
22.3 VISION
ommatidia along the dorsal rim of each eye (Meyer &
Labhart, 1993). These polarization sensitive ommatidia Field of view Insects with well-developed compound eyes
constitute only 6.6% of the total ommatidia in generally have an extensive field of view. For example, in
Cataglyphis, and 2.5% in Apis. the horizontal plane Periplaneta has vision through 360 º,
VISION 601
a)
b)
ultraviolet ultraviolet
sensitive sensitive
c) stimulus
plane of
polarization
o
0
60 o
o
80
1s
Fig. 22.15. Detection of the plane of polarization. (a) Arrangement of microvilli in the rhabdom in the polarization-sensitive
area. Six of the eight retinula cells are ultraviolet-sensitive with orthogonally arranged microvilli (Cataglyphis) (after Wehner,
1982). (b) Orientation of the rhabdoms in the polarization-sensitive area along the dorsal margin of the right eye of
Cataglyphis (after Wehner, 1989). (c) Response of an interneuron in the medulla to stimulation of the eye with light polarized
in different planes. Vertically polarized light (0°) results in depolarization of the interneuron and an increase in its firing rate.
Near horizontally (80°) polarized light causes a hyperpolarization and inhibition of the cell. These effects are thought to be
produced by interaction of the input from retinula cells with different microvillar orientation, as in (a) (Gryllus) (after
Labhart, 1988).
with binocular vision in front and behind the head (Fig. Many insects have binocular vision in front of the head
22.16). In the vertical plane the visual fields of the two eyes and so have the potential to assess distance stereoscopically.
overlap dorsally, but not ventrally (Butler, 1973). The This depends on the angle which the object subtends at the
visual fields of grasshoppers and many other insects are two eyes (Fig. 22.17). Errors can arise in the estimation of
similar to that of the cockroach. distance due to the size of the interommatidial angle, as
this is important in determining resolution. Fig. 22.17
Distance perception Insects are able to judge distance with shows the error of estimation which might arise if the
considerable accuracy. This is most obvious in insects, interommatidial angle was 2 º; larger interommatidial
such as grasshoppers, that jump to a perch, or in visual angles will result in greater errors. Errors will also be larger
predators like mantids, but is also true for any insect if the distance of the insect from its prey is long relative to
landing at the end of a flight. Two possible mechanisms the distance between the eyes, and in many carnivorous
exist that enable insects to estimate distance: a stereoscopic insects which hunt visually, such as mantids and
mechanism and motion parallax. Zygoptera, the eyes are wide apart.
602 VISION
a) vertical b) horizontal
binocular
vision binocular
vision
possible
error
compound anterior
eye
blind binocular
area vision
Fig. 22.16. Visual field of Periplaneta (after Butler, 1973). (a) In projection of 2 o
the vertical plane, the visual fields of the two eyes overlap above interommatidial
angle
the head giving binocular vision. (b) In the horizontal plane, the
visual fields of the two eyes overlap in front of and behind the
head giving binocular vision in both directions.
slow
movement
60 60
30 30
0 0
0 5 10 0 3
b) patterned background
90
b) horizontal patterns
angular movement (o )
0
0 5 10
time (seconds)
a) hair beds b)
compound
eye
corneal
lens
lateral
ocellus pigment
cell
rhabdoms
median
ocellus
synaptic
plexus
frons ocellar nerve
giant
lens would bring interneuron
image to a focus at
this point
Fig. 22.20. Ocellus. (a) Frontal view of the head of a grasshopper showing the positions of the ocelli. (b) Diagrammatic
longitudinal section through an ocellus of a grasshopper. The diagram shows the light-adapted condition with the pigment of
the pigment cells restricting the entry of light. Notice that the image is focused below the rhabdoms (after Wilson, 1978).
occupy a more dorsal position on the vertex. The median terminates in a synaptic plexus immediately behind the
ocellus shows evidence of a paired origin as the root of the ocellus. Two anatomical classes of ocellar interneurons
ocellar nerve is double and the ocellus itself is bilobed in originate here. Some have giant axons, up to 20 m in
Odonata and Bombus (Hymenoptera). Frequently, one or diameter (often called large (L) fibers), others are of small
all of the ocelli are lost and they are often absent in wing- diameter (S fibers). About 10 large fibers and up to 80
less forms. small ones are associated with each ocellus. In most insects
A typical ocellus has a single thickened cuticular lens studied, the large interneurons end in the brain, but in
(Fig. 22.20b), although in some species, such as bees and flies some extend to the thoracic ganglia (Fig.
Schistocerca and Lucilia, the cuticle is transparent, but not 22.21). Where these descending interneurons are absent,
thickened, and the space beneath it is occupied by trans- the pathway to the thoracic motor centers is completed by
parent cells. Each ocellus contains a large number of ret- second order descending interneurons. The small inter-
inula cells packed closely together without any regular neurons connect with several other centers in the brain,
arrangement; in the locust ocellus there are 800–1000. A including the optic lobes, mushroom bodies and the
rhabdomere is formed on at least one side of each retinula central body.
cell, and the rhabdomeres of between two and seven cells The retinula cell axons synapse repeatedly and recipro-
combine to form rhabdoms. The rhabdomeres usually cally with each other and with the interneurons which also
occupy much of the cell boundary and, in the case of synapse with each other. Some of the synapses between
Rhodnius, are present all round the cells, forming a hexago- interneurons and retinula cells are input synapses to the
nal meshwork similar to that in the stemmata of Cicindela retinula cells indicating that the interneurons may modu-
(see Fig. 22.23c). The structure of the rhabdomeres in the late the activity of the retinula cells as well as receiving
dorsal ocelli is the same as that in the compound eye. information from them.
Pigment cells sometimes invest the whole ocellus, but Illumination produces a sustained depolarization of
in some species, like the cockroach, are lacking. A the retinula cell which is proportional to light intensity.
reflecting tapetum, probably consisting of urate crystals in No action potentials are produced in the retinula cells,
a layer of cells, may be present at the back of the receptor and graded receptor potentials are transmitted along the
cells. axons to the synapses. As at the first synapses behind the
Each retinula cell gives rise, proximally, to an axon compound eye, the signal is amplified and the sign is
which passes through the basal lamina of the ocellus and reversed. Also as in the compound eye, the input signals
STEMMATA 605
subesophageal
ganglion
22.5 STEMMATA
7
corneagen
head cell
capsule corneal
lens 3
distal
corneagen 1 rhabdom
cell 2
crystalline envelope
lens 5 cells
distal
2 1 rhabdom corneagen
cell
proximal 3 7
stemmata 6 4 rhabdom 6
1 proximal
4 rhabdom
2 5
antenna envelope
cells envelope
cells
Fig. 22.22. Stemmata with a single rhabdom in a caterpillar (mainly after Ichikawa & Tateda 1980). (a) Side of the head
showing the positions of the stemmata. (b) Longitudinal section of one stemma. (c) Transverse sections through the distal
and proximal rhabdom.
angles of the distal rhabdomeres are close to 10 ° so that spatial resolution in these eyes is limited because of optical
they have low spatial resolution. The proximal rhab- pooling and perhaps electrical coupling (Toh & Mizutani,
domeres have much smaller acceptance angles, of less than 1994).
2 °. This, together with the fact that the focal plane of the The optic lobes of larval insects consist of a lamina and
lens is at the level of the proximal cells, gives them better medulla comparable with those associated with compound
spatial resolution. The visual fields of adjacent stemmata eyes of adults and, at least in caterpillars, each stemma
do not overlap so the caterpillar perceives an object as a connects with its individual cartridge in the lamina.
very coarse mosaic, which is improved by side-to-side In all these types of stemmata, the retinula cells contain
movements of the head enabling it to examine a larger screening pigment granules in addition to the visual
field. It is known that caterpillars can differentiate shapes pigment. Movement of the granules, away from the rhab-
and orient towards boundaries between black and white domeres in the dark and towards them in the light, pro-
areas (Ichikawa & Tateda, 1982). vides sensitivity adjustment.
The situation is different in larval symphytans Caterpillars have three visual pigments and the neural
(Hymenoptera), which have only a single stemma. These capacity to distinguish colors and the larvae of several
have large numbers of rhabdoms each formed by eight ret- holometabolous species have been shown, experimentally,
inula cells and each group of cells is isolated by pigment to respond to the plane of polarization of incident light. In
from its neighbors. The lens produces an image on the tips neither case is the behavioral importance of these abilities
of the rhabdoms which, in Perga, are oriented at about 5 ° understood.
from each other (equivalent to the interommatidial angle Review: Gilbert, 1994
in compound eyes). Consequently, this type of eye is
capable of moderately good form perception (Meyer-
22.6 OTHER VISUAL RECEPTORS
Rochow, 1975).
The larvae of the tiger beetle, Cicindela, have six stem- 22.6.1 Dermal light sense
mata, like caterpillars, but with a large number of retinula A number of insects, such as Tenebrio larvae, still respond
cells in each stemma, as in the Hymenoptera. The largest to light when all the known visual receptors are occluded.
of the stemmata has about 5000 retinula cells each of which The epidermal cells are apparently sensitive to light. This
forms a rhabdomere on all sides so that the rhabdoms are is also suggested by the pigment movements which occur
in the form of a lattice (Fig. 22.23). It is possible that in isolated epidermal cells of some insects (section 25.5.1),
REFERENCES 607
and by the production of daily growth layers in the cuticle phaosomes and they probably monitor the positions of the
(section 16.2.1.1). genitalia during copulation (Miyako, Arikawa & Eguchi,
Several families of butterflies are known to have photo- 1993).
receptors on the genitalia of both sexes. In Papilio, there
are two receptors on each side, each consisting of a single 22.6.2 Sensitivity of the brain
neuron lying on a nerve a short distance below the epi- In several insect species, light affects neural activity
dermis. The cuticle above the neuron is transparent. The directly by acting on the brain, not via the compound eyes
cell extends into a number of processes and from these or ocelli. This commonly occurs in the entrainment of
large numbers of microvilli arise. These are closely packed diurnal rhythms. In some species, daylength, regulating
together, without any particular orientation, and appear to diapause or polyphenism, is registered directly by the
be contained within the cell, but are probably formed from brain. The light-sensitive structures are not known,
the cell membrane as they are in similar light-sensitive although possible candidates have been described in tene-
structures in other invertebrates. The cells are called brionid beetles (Fleissner, Fleissner, & Frisch, 1993).
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23 Mechanoreception
Mechanoreception is the perception of any mechanical wall of the hair consists of exocuticle with an outer layer of
distortion of the body. This may result from touching an epicuticle.
object or from the impact of vibrations borne through the Most commonly, the hairs taper from base to tip, and
air, water or the substratum, and thus mechanoreception they are often known as trichoid sensilla (this term also
includes the sense of hearing. It also includes distortions applies to chemoreceptors with a similar form). Others, on
of the body which arise from the stance of the insect and the cerci of crickets and cockroaches, for example, are very
from the force exerted by gravity, so some mechanorecep- long relative to their diameter and do not taper; they are
tors are proprioceptors. Three broad structural categories called trichobothria. Some insects, such as first stage
of mechanoreceptor are present in insects: cuticular grasshoppers, have club-shaped hairs, and the position-
structures with bipolar neurons; subcuticular structures sensitive hairs on the cerci of some cockroaches consist of a
with bipolar neurons, known as chordotonal organs; sphere of cuticle on a short stalk. Other forms occur in
internal multipolar neurons which function as stretch relation to specific functions.
receptors. Whatever the external form, the hair-like structure
Definition: The term sensillum (plural: sensilla) refers to arises from a socket permitting movement of the hair, and
the basic structural and functional unit of cuticular neural stimulation results from the displacement of the
mechanoreceptors and chemoreceptors. It includes the hair in its socket. To give this flexibility and hold the hair
cuticular structure, the neuron or neurons, the associated in its normal position, the socket usually has three compo-
sheath cells with the cavities they enclose and the struc- nents (Fig. 23.1). Externally, a thin cuticular joint mem-
tures they produce. Fig. 23.1 shows the basic elements of a brane is continuous with the general body cuticle and that
sensillum. Sensilla often occur singly, but may also be of the hair. Beneath this, bridging a gap between the body
grouped together to form functional units. cuticle and the hair, are rings of suspension fibers. Finally,
Review: McIver, 1985 on the inside, is the socket septum. This is also fibrous, but
appears more delicate than the suspension fibers. It runs
across the outer part of the receptor lymph cavity to the
23.1 CUTICULAR MECHANORECEPTORS
dendrite sheath.
Cuticular mechanoreceptors fall mainly into two classes: These suspensory structures restore the hair to its orig-
hair-like projections from the cuticle with a basal socket, inal position following movement. They often also restrict
and dome-like campaniform sensilla. Both types have the extent to which the hair can be moved in different
similar arrangements of neurons and sheath cells. directions, so it is common for hairs to have directional
sensitivity. Directional sensitivity is also conferred by the
23.1.1 Structure position at which the dendrite is inserted into the hair base
23.1.1.1 Cuticular components (see Fig. 23.5b).
Hair-like structures Most of the larger hairs on an insect’s In addition to scattered mechanoreceptor hairs, all
body are mechanoreceptors. There are no pores (apart insects have groups of small hairs, known as hair plates, at
from the molting pore, see below) in the cuticle of hairs some joints in the cuticle.
that function solely as mechanoreceptors, and they are,
therefore, known as aporous sensilla. Many contact Campaniform sensilla Campaniform sensilla are areas of
chemoreceptors also have a mechanoreceptor function thin cuticle, domed and usually oval in shape with a long
and, although they have a terminal pore, it is not relevant diameter usually in the range 5–30 m. The dome of thin
to the mechanoreceptive function (section 24.2.1). The cuticle consists of an outer homogeneous layer with the
[610]
CUTICULAR MECHANORECEPTORS 611
ciliary region
receptor lymph
cavity
proximal
dendrite thecogen cell
trichogen cell
tormogen cell
soma
epidermal cell
fibrous cuticle
exocuticle
distal dendrite
dendrite sheath
endocuticle
receptor lymph
cavity
tormogen cell
appearance of exocuticle, and an inner lamellar or fibrous position of the sensillum even within a species. Grünert &
layer (Fig. 23.2). Sometimes these two layers are separated Gnatzy (1987) recognize nine different types in adult
by a layer of transparent (in the electron microscope) Calliphora.
cuticle referred to as spongy cuticle. The dome is con- Campaniform sensilla are situated in areas of the
nected to the surrounding cuticle by a different type of cuticle that are subject to stress. On the appendages, where
cuticle. It is called the joint membrane. The dendrite they occur most commonly, they are usually close to the
sheath, enclosing a single dendrite, is inserted into the joints. Fig. 8.7a shows their distribution on one leg of a
center of the dome, and a molting pore may be visible on cockroach. In some orthopteroid insects, there is a single
the outside. Details of the structure vary according to the campaniform sensillum at the base of each of the tibial
612 MECHANORECEPTION
max
sensitivity
completely
insensitive
0 20 40 60 80
time (hours)
Fig. 23.3. Sensitivity of a hair sensillum in relation to molting. Diagrams in the upper panel illustrate the structural changes
occurring through one larval stage from one ecdysis (time 0) to the next (compare Fig. 16.17). Lower panel shows the
sensitivity of the hair to stimulation at different times. Sensitivity is completely lost only for about 30 minutes at ecdysis
(partly based on Gnatzy & Tautz, 1977).
spines. Campaniform sensilla also occur on the mouth- breaking off at ecdysis. The point of breakage is marked on
parts, on the basal segments of the antennae, on veins close the outside of the sensillum by a molting pore (Figs. 23.1,
to the wing base, and on the ovipositor, while large 23.2). During the molt the sheath presumably protects the
numbers are present on the haltere of Diptera (Figs. 9.14, dendrites from enzymes in the molting fluid, making it
9.15). An adult Calliphora has a total of approximately possible for the sensillum to continue functioning after
1200 campaniform sensilla, about 36 on each leg, 140 on apolysis until the time of ecdysis. In caterpillars of
each wing base and 340 on each haltere (Gnatzy, Grünert Barathra, for example, the sound-sensitive hairs are non-
& Bender, 1987). They often occur in groups, all those functional for only about 30 minutes before ecdysis and the
within a group having the same orientation and, presum- new hair is functional within a few minutes of the old
ably, functioning as a unit. cuticle being shed (Fig. 23.3).
response
23.1.3.1 Exteroception
Hair sensilla responding to external stimuli are usually
phasic. They are concerned with the sense of touch and
c) phasic/tonic response
sometimes with sensing air movement and with orienta-
tion with respect to gravity.
instantaneous firing rate
400
(action potentials.s -1)
Amongst Orthopteroid insects, hairs sensitive to air a) directional mobility b) directional sensitivity
movement are present on the cerci and they are also
responsive to sounds in some cases. Hairs responding to base of hair
airborne vibration are usually long and slender, and have
flexible mounting in the sockets so that they vibrate freely.
Whereas tympanal organs respond to changes in air pres-
sure associated with a sound (see below), hair sensilla are
particle movement receptors, responding to movements of
the air created by the sound source. Because the energy hair
associated with particle displacement falls off rapidly with c) frequency sensitivity base
dendrite
insertion
distance from the source, these receptors usually function 50
displacement (µm)
near field. This is often no more than a few centimeters
(see Ewing, 1989; Michelsen & Larsen, 1985). 25
a)
nerve sensory neurons
trachea
connecting with
pressure epidermis
receptors on
other segments
spiracle
cuticle
sensory water
papilla
mushroom mushroom sensilla airspace -
sensillum forming a continuous continuous with
layer tracheal system
b)
ANTERIOR POSTERIOR
trachea
insect horizontal
pressure
receptor
water
pressure
layer of mushroom
sensilla abdomen above
head
mushroom layer
pushed out by air
in tracheae
mushroom layer pushed
in by water pressure
head above
abdomen
mushroom layer
pushed out by air
in tracheae mushroom layer pushed
in by water pressure
Fig. 23.6. Pressure reception by the water scorpion, Nepa (Hemiptera) (after Thorpe & Crisp, 1947). (a) Diagram of the
receptor system associated with one spiracle on the ventral surface of the abdomen. The overlapping ends of the mushroom
sensilla form a continuous flexible sheet holding an airspace which is continuous with air in the tracheal system. (b) Diagram
showing how the pressure receptors of adjacent spiracles are joined through the tracheal system and the manner in which
pressure differences arising when the body is tilted cause differential movements of the mushroom sensilla.
which are thus stimulated. The insect responds to such an abdominal segments three to five. Each consists of over
increase in pressure by swimming up, but there is no 100 hair sensilla whose tips are expanded into thin plates
response to a decrease in pressure (Thorpe & Crisp, 1947). giving them a mushroom-like appearance. The plates of
Pressure receptors are also present in Nepa adjacent sensilla overlap and enclose an airspace (Fig.
(Heteroptera) which has a pair on the sternum of each of 23.6a). A spiracle opens into the space and the spaces in the
CHORDOTONAL ORGANS 617
three organs of one side are connected through the tra- cuticle of distal
cheal system. The receptors give no general response to an segment
increase in pressure, but differential stimulation of the
organs of one side does produce a response. If the head is hair plate
tilted upwards, the air in the system tends to rise towards sensilla
the head end and the anterior mushroom-shaped plates membranous
tend to be pushed out while those on the posterior organ cuticle of joint
collapse (Fig. 23.6b). The converse is true if the head is hemocoel
tilted downwards. The resulting sensillar movements
enable the insect to determine its orientation. The role of muscle
the sensory papillae shown in Fig. 23.6 is unknown cuticle of proximal
(Thorpe and Crisp, 1947). segment
23.1.3.2 Proprioceptors Fig. 23.7. Diagram showing how the sensilla of a hair plate are
Trichoid sensilla Groups or rows of small hairs often stimulated by coming into contact with adjacent cuticle.
occur at joints between some leg segments (see Fig. 8.7a),
on the basal antennal segments, on the cervical sclerites Campaniform sensilla usually occur in groups and are
and elsewhere. They monitor the position of one cuticular oriented at right angles to the principal lines of stress (see
element relative to another. The hairs are positioned so Fig. 8.7a). For example, the campaniform sensilla on the
that the flexing of one part of the cuticle with respect to leg are so oriented that they are stimulated when the foot is
another causes the hairs to bend (Fig. 23.7). Often the on the ground and the leg bears the insect’s weight.
hairs in a hair plate (or hair bed) are graded in size, pre- Sensilla with different orientations are sensitive to bending
sumably giving the potential to discriminate between in different directions as the insect’s stance changes or
different degrees of flexion. different muscles become active.
Hair plates on the first cervical sclerite and on the front Input from campaniform sensilla on the legs forms part
of the prothorax provide the insect with information about of a negative feedback loop producing reflex changes in
the position of its head relative to the thorax. This is par- muscle tension (Schmitz, 1993). When a group of cam-
ticularly important in the mantis during feeding and also paniform sensilla is stimulated, their input leads to a
aids the stability of the locust in flight when the head is ori- reduction in neural output to a muscle exerting stress on a
ented by a dorsal light reaction and the thorax is aligned leg. As a result, muscle tension falls, the stress on the leg is
with the head (section 9.11.2). reduced, and the campaniform sensilla are no longer
Hair plates are also important in orientation with stimulated. Such effects are probably continuously in
respect to gravity because the extent to which the hairs are operation, enabling the insect to maintain its stance or
stimulated will depend on the insect’s orientation. They adjust leg movements during walking.
are probably the principal gravity receptors in most terres-
trial insects. Those on the legs are of particular impor-
23.2 CHORDOTONAL ORGANS
tance, but others at the bases of the antennae also
contribute. Several different hair plates probably contrib- 23.2.1 Structure
ute to the response at any one time, although one group Chordotonal, or scolopophorous, organs consist of single
may be dominant. In the stick insect, Carausius, hair plates units or groups of similar units called scolopidia. They are
on the trochantin which are stimulated by the coxa are of subcuticular, often with no external sign of their presence,
principal importance. and are attached to the cuticle at one or both ends. Each
scolopidium consists basically of three cells: the neuron,
Campaniform sensilla In the insect skeleton all stresses an enveloping, or scolopale cell, and an attachment cell
can be expressed as shearing stresses in the plane of the (Fig. 23.8). Some scolopidia contain more than one
surface. Such stresses produce changes in the shape of the neuron. The dendrite narrows to a cilium-like process
campaniform sensilla resulting in their stimulation. The containing a peripheral ring of nine double filaments and
response is phasic/tonic. with roots extending proximally within the dendrite. In
618 MECHANORECEPTION
scolopale
cell
neuron
soma
glial cell
axon
some scolopidia, and perhaps in all, the doublets are con- 23.2.2 Functioning
nected with the cell membrane near their origins at the The coupling mechanism by which external movement is
basal body by a structure called the ciliary necklace transmitted to the dendrite probably varies in different
because of its appearance. In some scolopidia, the tip of the chordotonal organs, but where the organ bridges the junc-
cilium lies in a hollow of the extracellular scolopale cap. In tion between two cuticular plates, movements of one rela-
others, the dendrite dilates distal to the cilium. The tive to the other distort the scolopidium. Where the
scolopale cell contains the scolopale which consists of scolopidium is only connected with the cuticle at one end,
fibrous material containing actin arranged in a ring or a other factors are responsible for the distortion (see below).
series of rods (Wolfrum, 1991). The ciliary region of the Whatever the origin of the distortion, the effect is perhaps
dendrite lies in an extracellular space within the folds of to displace the scolopale cap producing sliding of the tubule
the scolopale cell. The contents of the extracellular space doublets which leads to bending at the base of the cilium.
are not known. The attachment cell connects the sensillum The actin of the scolopale may be involved in restoring the
to the epidermis. position of the cap and dendrite after bending.
CHORDOTONAL ORGANS 619
hair
base of
flagellum
scolopidia of
outer ring
pedicel
scolopidia of Johnston's
inner ring organ
basal plate
single
scape scolopidia
scolopidia which extend from the scape to the flagellum. orientation in the water. In this species, an air bubble
The males of these insects have plumose antennae with extends between the head and the antenna so that when the
many fine, long hairs arising from each annular joint. insect is correctly orientated on its back the antenna is
These hairs are caused to vibrate by sound waves and their deflected away from the head. If, however, the insect is the
combined action produces a movement of the flagellum. wrong way up the antenna is drawn towards the head and
The amplitude of flagellar movement is greatest near its Johnston’s organ registers the position.
own natural frequency which approximately corresponds
to the flight tone of the mature female and stimulation at 23.2.3.3 Tympanal organs
this frequency leads to the seizing and clasping response in Structure and occurrence of tympanal organs Tympanal
mating. Aedes aegypti males are most readily induced to organs are chordotonal organs specialized for sound recep-
mate by sound frequencies between about 400 and 650 Hz, tion. Each consists of an area of thin cuticle, the tympa-
but the limits to which they respond become wider as the num (or tympanic membrane), which is generally backed
insect gets older and are wider in unmated than in mated by an air-sac so that it is free to vibrate. Attached to the
males. Sounds at other frequencies and high intensities inside of the tympanum or adjacent to it is a chordotonal
produce a variety of reactions: cleaning movements, organ which contains from one scolopidium, in Plea
jerking, flight or becoming motionless. (Heteroptera), to over 1000 in some Cicadidae. Tympanal
Gyrinid beetles are able to perceive ripples on the water organs occur on the neck membrane of some scarab beetles
surface, apparently due to displacements of the antennal (Forrest et al., 1997), on the prothoracic legs of Grylloidea
flagellum, so that they are able to avoid collisions with and Tettigonioidea, on the prothorax of at least one para-
other insects and, by echolocating using their own ripples, sitic fly (Robert, Read & Hoy, 1994), on the mesothorax of
also avoid the sides of their container. In order to do this, some Hydrocorisae, such as Corixa and Plea, on the meta-
the insect must also be able to detect the direction from thorax in Noctuoidea, and on the abdomen in Acrididae,
which the ripples are coming. Cicadidae, Pyralidoidea and Geometroidea (Lepidoptera)
Johnston’s organ probably also contributes input rele- and Cicindellidae (Coleoptera) (Spangler, 1988a). In
vant to an insect’s orientation with respect to gravity, and, Chrysopa (Neuroptera) the tympanum is on the ventral
in the water boatman, Notonecta, it is concerned with side of the radial vein of the forewing.
622 MECHANORECEPTION
Acrididae (grasshoppers) have a tympanum in a recess 23.13b). It is called the crista acoustica, and, in Decticus, it
on either side of the first abdominal segment (Fig. 23.12). contains 33 scolopidia which lie parallel with each other in
It is about 2.5 ⫻1.5 mm2 in area in adult Locusta, varying a vertical row, the sensilla becoming progressively smaller
in thickness from less than 1 m to over 10 m. Most of its towards the distal end (see Fig. 23.17). In Teleogryllus they
cuticle is weakly sclerotized mesocuticle, but small islands are within a tent-like membrane which extends along the
of well sclerotized cuticle serve for the attachment of tympanal organ between the wall of the trachea and the
different groups of scolopidia. The cuticle of the airsac dorsal wall of the tibia. The neuron somata lie on the wall
which backs the tympanum is only 0.2 m thick and of the trachea and the dendrites project into the cavity of
perhaps consists only of epicuticle. The chordotonal the tent. More proximal scolopidia are attached to large
organ, known as Muller’s organ, is complex, containing, in accessory cells within the tent, but, more distally, long
Locusta, about 80 neurons with their cell bodies aggre- attachment cells extend directly to the tibial epidermis. In
gated into a ganglion. From the ganglion, the sensory units these insects, as in the Acrididae, tympanal organs are
connect with the tympanum in four separate groups with present in all the larval stages, but they probably only
different orientations (shown by arrows in Fig. 23.12b). become functional in the later larvae and adults.
The whole chordotonal organ and the auditory nerve The tympanal organs of the Noctuoidea occupy the
which runs from it to the metathoracic ganglion are posterior part of the metathorax (Fig. 23.14) and the tym-
enclosed in folds of the airsac which backs the tympanum. panum faces into a space between the thorax and abdomen
Airsacs are contiguous right across the body between the roofed over by the alula of the hind wing. Medial to the
two tympani. tympanum, and resembling it structurally, is a second
The tympanal organs of Grylloidea (crickets) and membrane, but it has no sense organ. This second mem-
Tettigonioidea (bushcrickets) are similar to each other in brane is the counter tympanic membrane, and is probably
basic structure, being situated in the base of the fore tibia, an accessory resonating structure. The sense organ
which is slightly dilated and typically has a tympanum on attached to the back of the tympanum contains only two
either side, anterior and posterior with the leg at right scolopidia, supported by an apodemal ligament and an
angles to the body (Fig. 23.13a). Often the posterior tym- invagination of the tympanal frame.
panum is bigger than the anterior one and sometimes, as in In cicadas the two tympani are situated ventro-laterally
Gryllotalpa, only the former is present. In most on the posterior end of the first abdominal segment behind
Tettigonioidea, the tympanic membranes are enclosed by the folded membrane and beneath the operculum (see Fig.
forwardly projecting folds of the tibial cuticle with only a 26.10). The air-sacs by which they are backed are continu-
narrow gap connecting to the outside. ous right across the abdominal cavity. Each chordotonal
In both crickets and bushcrickets, the cavity of the leg organ contains about 1000 scolopidia enclosed in a cut-
between the two tympani is almost entirely occupied by a icular tympanic capsule and attached to the posterior rim
trachea divided into two by a rigid membrane, the blood of the tympanum by an apodeme.
space of the leg being restricted to canals anteriorly and In Chrysopa, the tympanum is on the ventral side of the
posteriorly (Fig. 23.13b). In tettigoniids, the trachea runs radial vein of the forewing. This vein has a bulbous
proximally through the femur without branching and swelling near the base that is thick walled and rigid above,
widens into a vestibule opening at the prothoracic spiracle. but has the thin tympanum below. Unlike most other tym-
Its cross-sectional area changes from tibia to spiracle in a panal organs, the tympanum is in direct contact with the
way that approximates the shape of an exponential horn so hemolymph; it is not backed by an air-sac. About 28 scolo-
that sound entering the spiracle is amplified. This trachea pidia are associated with the tympanum.
is isolated from other tracheae and the spiracle has no
closing mechanism. In crickets the trachea does not Functioning of the tympanal organs Sound impinging
expand in this way, but the tracheae of the two sides join on the tympanic membrane causes it to vibrate, the ampli-
across the midline (see Fig. 23.15) although the airspaces tude of the vibrations varying with the intensity of sound
are separated by a delicate septum. and the structure of the membrane. In Locusta, different
The chordotonal organ associated with the tympanal parts of the membrane vibrate to some extent inde-
organs is in the anterior hemocoelic space of the tibia (Fig. pendently of each other. Vibration is also affected by the
CHORDOTONAL ORGANS 623
a) horizontal section
flight muscles
cuticle of
metathorax
first abdominal
spiracle Muller's
trachea organ
communicating
with airsac tympanum
airsacs
gonad cuticle of first
abdominal
segment
pyriform vesicle
cuticular rim
inner face of
tympanum styliform body
elevated process
b fusiform body
a pyriform vesicle
ganglion
d
folded body 8 4 2 1
cut edge of 10
c tympanum
20
auditory
nerve
Fig. 23.12. Tympanal organ of a grasshopper. (a) Diagrammatic horizontal section through the metathorax and first
abdominal segments showing the positions of the tympanal membranes. Notice that the airsacs form a continuum across the
body (Oedipoda) (from Schwabe, 1906). (b) Diagram showing the attachment of the scolopidia to the inside of the tympanum.
The cuticle of the airsac which normally covers Muller’s organ and the tympanum has been removed. The orientations of
scolopidia in different parts of the chordotonal organ are indicated by arrows. Letters show the positions of cells some of
whose sensitivities are shown in Fig. 23.17a. The styliform body, elevated process and folded body are cuticular structures
continuous with the tympanum (Locusta) (after Gray, 1960). (c) Thickness of the tympanum. Lines mark contours of
thickness and numbers show the thickness in microns. Hatched areas are regions of well-sclerotized cuticle (Schistocerca)
(after Stephen & Bennet-Clark, 1982).
624 MECHANORECEPTION
membrane dividing
auditory trachea
cuticle of auditory
tibia trachea
posterior (ventral)
blood space nerve trachea
muscle
b) chordotonal organs
trachea
sensory
neurons auditory nerve
subgenual scolopale
organ cells
attachment sensory
cells neurons
scolopale intermediate
cells organ
attachment
proximal scolopidia cells
of crista acoustica
level of section
in a
sensory
neurons crista
acoustica
attachment
cells
tympanic cavity
tympanic cavity
anterior face of
auditory trachea
cuticle of
tibia
CHORDOTONAL ORGANS 625
airsac
axons from ligament
scolopidia
tympanum
counter tympanic
membrane tympanic
chordotonal recess
organ abdomen
degree of damping of the tympanum. In most insects this bushcrickets, high frequency sound (above 20 kHz) enter-
damping is reduced to a low level by the air-sacs backing ing the prothoracic spiracle (Fig. 23.15a) is amplified in the
the tympanum, but the locust tympanal membrane is tracheal horn so that it dominates the vibrations induced in
damped to some degree by the mass of Muller’s organ and the tympanic membrane which acts as a pressure receiver.
sensitivity may be further reduced if the fat body is well At low frequencies, however, relatively little amplification
developed. occurs and the tympanum acts as a pressure difference
Tympanal organs may be pressure receivers, in which receiver (Michelsen, Popov & Lewis, 1994b).
sound impinges only on one side of the tympanum, or In crickets, because the tympanal organs of left and
pressure-gradient (pressure-difference) receivers, in right legs are connected via the transverse trachea, each
which sound reaches both sides of the membrane. In the tympanum may receive sound via four routes: directly
latter, vibration of the tympanum depends on differences from the outside, or indirectly via the ipsilateral spiracle,
in sound pressure on its two sides resulting from the contralateral spiracle, or the contralateral tympanum
differences in phase of the vibrations. The sound reaching (Fig. 23.15b). At the frequency of the calling song, about
the inner face of the tympanum is not the same as that 4.7 kHz, the last is relatively unimportant, but the input
reaching the outside because some frequencies may be via both spiracles is essential for the insect’s directional
differentially absorbed in transit through the system, sensitivity (see below, and Michelsen et al., 1994a).
which acts as a filter, or because the intensities of some fre-
quencies are amplified more than others. For clear LOUDNESS. The number of action potentials produced
accounts of the physical principles involved see Ewing by the neuron of a scolopidium is proportional to the
(1989) and Michelsen & Larsen (1985). intensity or loudness of the sound (Fig. 23.16). The
In insects, sound can reach the inner side of a tympanum response threshold for a single neuron varies according to
via the tracheal system or through the tissues, but, because the sound frequency, and different scolopidia within the
the intensity and phase of the sound reaching the inside of same chordotonal organ may have different thresholds.
the tympanum depends on frequency, each tympanum can When sound intensity is very high, the response saturates;
function either as a pressure receiver or as a pressure no further increase is possible. Between threshold and
difference receiver. The change from one to the other saturation is the dynamic range in which the magnitude of
occurs at about 10 kHz in locusts. At frequencies below this, the response is a measure of sound intensity. The dynamic
sound reaches the tympanum from both sides and it func- range of a neuron is often around 30 dB, but cells with
tions as a pressure difference receiver. At frequencies above different thresholds extend the dynamic range for the
10 kHz, most sound reaches the tympanum from the insect. This is most obvious in noctuid tympanal organs in
outside because sound entering the airsacs is filtered out which there are only two scolopidia. These have similar
and so the tympanum functions as a pressure receiver. In frequency responses but their thresholds differ by about
626 MECHANORECEPTION
a) bushcricket
prothoracic
horn-shaped spiracle
trachea
femur
tympanum
tibia weak or
occluded
connection
a) locust
80
c a
sound intensity (dB)
c
d b bushcricket
a
60 d proximal distal
40
1 2 5 10 20 40 80
c) noctuid moth
40
100
sound intensity (dB)
80
1 2 5 10 20
A2 cell
60 sound frequency (kHz)
A1 cell
40
20
10 20 50 100
sound frequency (kHz)
Fig. 23.17. Frequency thresholds of individual scolopidia in tympanal organs. Note that the lowest threshold equates with the
highest sensitivity. Bold arrows at the top indicate the approximate upper limit of human hearing (about 15 kHz). (a) A locust.
Letters, a, c and d, refer to the groups of scolopidia with the same lettering in Fig. 23.12b. Hatched areas show the range of
sensitivities of different cells in the same group (after Michelsen & Nocke, 1974). (b) A bushcricket. Above: the crista
acoustica. Below: responses of scolopidia at different distances along the crista acoustica. The more distal the scolopidium,
the higher the frequencies to which it responds. Notice that cells responding to the highest and lowest frequencies are very
insensitive, responding only at high sound intensities (after Oldfield, 1982). (c) A noctuid moth. The two scolopidia in the
chordotonal organ respond to a wide range of frequencies, but cell A1 is much more sensitive than cell A2 (after Waters &
Jones, 1996).
input in the tympanal nerve, representing the sum of Some of the interneurons relaying information to the
membrane oscillation and the sensitivity of the sensory brain are tuned to specific frequencies. One such inter-
neurons, is maximal at 5–10 kHz, with a second maximum neuron in Ancistrura has a maximum response to stimula-
between 25 and 35 kHz. tion of the tympanum by frequencies in the range
In bushcrickets, the intermediate organ may be respon- 12–16 kHz, corresponding with the principal frequencies
sible for the perception of low frequency sound, while, in in the male song. The interneuron is inhibited by sound
the crista acoustica, proximal scolopidia are most sensitive frequencies above and below this range (Stumpner, 1997).
to low frequencies and more distal cells to higher frequen-
cies (Fig. 23.17b). This tuning is not due to differences in PULSE RATE. Sound communication among insects
the tympanum, and is perhaps a property of the individual often depends on the production and reception of discrete
scolopidium, although this has not been demonstrated. pulses of sound (section 26.3.1). The ability to distinguish
628 MECHANORECEPTION
directional sensitivity. Noctuids are able to locate a source above). Directional sensitivity is obviously a critical
of high frequency sound when they are flying and so they element in these behaviors.
have to localize sounds in a vertical as well as a horizontal Sound is also important in predator avoidance and
direction. The wings tend to screen the tympani, so there insects in several groups have tympanal organs sensitive to
is a marked difference in the responses of the two organs to high frequency sounds. This is commonly assumed to
asymmetrical stimulation when the wings are raised, but relate to the avoidance of bats which emit high frequency
when the wings are in the lower half of their beat there is sounds, although in few cases is there strong evidence of
little difference between the two sides. When the wings are the importance of this behavior. Noctuid moths can detect
down the insect is more sensitive to sounds coming from bats about 30 m away and at such distances, where the
below it than to sounds from above. Thus, during flight, intensity of stimulation is low, tend to turn away from the
the auditory input from low intensity sounds of high fre- source of sound (see above). At high sound intensities,
quency will vary cyclically and in different ways according such as would occur when the bat was within about 5 m of
to the position of the sound source. the moth, it may close its wings and drop to the ground, or
The accuracy with which the insects orient to sound power dive to the ground, or follow an erratic, weaving
direction is not very great. If the sound source is within course.
about 10 ° of its body axis, the grasshopper, Chorthippus, Most of the scolopidia in the tympanal organs of
makes turns of up to 60 ° (sometimes more) to either side. cicadas are maximally sensitive in the range 1–5 kHz, well
If the angle of incidence is greater, the insect turns towards below the principle frequencies in the calling songs of
the correct side, but the turning angle is anywhere from 60 many species. It is possible that they are important in
to 120 ° irrespective of the angle of incidence. This often predator recognition.
results in the insect making a zigzag course towards the Some parasitic Diptera have been shown to use their
source because successive turns tend to put the sound auditory sense to locate their singing hosts. This has been
source on the opposite side of the body. Tettigoniids extensively studied in the case of Ornia, a parasitoid of
appear to orient more precisely, although still with consid- crickets (Robert et al., 1994), and it also occurs in
erable variation. Emblemasoma, a species which parasitizes cicadas (Soper,
Scolopidia may be stimulated by the insect’s own Shewell & Tyrrell, 1976).
normal activities. In Locusta, abdominal ventilation and Review: Bailey, 1991
flight may both modulate responses to sound, in some
cases completely inhibiting the response (Hedwig, 1988,
23.3 STRETCH RECEPTORS
1989).
Reviews: Ball, Oldfield & Rudolph, 1989 – crickets Stretch receptors differ from other insect mechanorecep-
Ewing, 1989; Hoy & Robert, 1996; Michelsen & Larsen, 1985; tors in consisting of a multipolar neuron with free nerve
Spangler, 1988b – moths endings, while all the others contain a bipolar neuron.
Stretch receptors have a variety of forms. Sometimes they
Functions of tympanal organs Insects have the capacity are an integral part of an oriented structure such as a
to hear many different sounds, including most sounds that muscle fiber or a strand of connective tissue, but in other
humans can hear (about 100 to 15 000 Hz), and, in those cases they have no specific orientation or associated struc-
with high frequency sensitivity, sounds that are not audible tures. In many cases, their function is inferred from light
to humans. Insects may respond behaviorally to such microscopy, or known from physiology without structural
sounds even though they are not the primary reason for the details.
insect’s auditory sense.
Orthoptera and cicadas produce sounds for attracting 23.3.1 Unspecialized receptors
mates and, in some species, for aggregation (section 26.5). Multipolar cells without an associated specialized struc-
Recognition of these sounds is dependent primarily on ture are often associated with epithelia. The cell body,
sound patterns rather than on variation in frequency, ensheathed in glial cells, is in the hemocoel, but the basal
although the hearing systems of different species respond lamina around the dendrites becomes fused with that of the
maximally to the frequencies of the sounds emitted (see epithelium. In the multipolar cells of the bursa copulatrix
630 MECHANORECEPTION
b) muscle
dendrite
a) glial cell
basal
lamina
epithelial
cell
attachment
varicosity of
dendrite
50 m
naked
branches of
dendrite
Fig. 23.19. Unspecialized stretch receptor on the outside of the bursa copulatrix of Pieris (after Sugawara, 1981). (a) The
epithelium of the bursa is covered by a layer of muscles. The soma of the multipolar neuron is free in the hemolymph,
although clothed by glial cells (not distinguishable in photograph). Dendritic endings of the stretch receptor pass between the
muscle strands and end on the surface of the epithelium. (b) Diagrammatic cross-sections of a dendrite beneath the muscle
layer. Top: it approaches the epithelium clothed by a glial cell. Middle: it swells to form a varicosity. Its basal lamina is
confluent with that of the epithelial cell beneath. Bottom: fine branches of the dendrite extend into the basal lamina of the
epithelial cell. They are no longer covered by a glial cell.
of Pieris, for example, each dendrite swells at intervals, the subepidermal nerve net, although they do not anastomose
swellings, with their basal lamina, apparently contributing to form a true net. These receptors monitor changes in
to the attachment. In this example, the finer dendritic body shape.
branches, free of glial covering, end in the basal lamina of Insects with a hard external cuticle are usually consid-
the epithelial cell (Fig. 23.19), but in fly larvae, the naked ered to have no subepidermal nerve net, but Knyazeva,
dendrites of stretch receptors on the epidermis end within Fudalewicz-Niemczyk & Rosciszewska (1980) report
invaginations of the epidermal cells. numerous multipolar neurons in the abdomen of the house
In soft-bodied dipterous larvae and perhaps in all cricket, Acheta. Blood-sucking insects have small numbers
insects with largely unsclerotized cuticle, multipolar cells of multipolar neurons beneath the abdominal epidermis.
are attached to the inside of the epidermis. The number of In adult tsetse fly, Glossina, there are three pairs of such
these neurons in cyclorrhaphan fly larvae is constant cells associated with the ventral body wall. They presum-
within a segment, varying from 24 in the prothorax to 30 in ably monitor abdominal distension when the insect feeds.
each of the abdominal segments. They collectively form a In Schistocerca, a few multipolar cells are present beneath
STRETCH RECEPTORS 631
the arthrodial membrane at the femoro-tibial joints. They the fiber, called the sarcoplasmic core, where, in the larva
respond to movement and position of the tibia with respect of Antheraea, a giant nucleus occurs (Fig. 23.20b).
to the femur (Williamson & Burns, 1978). Attached to the muscle is a tube of connective tissue
Some insects are known to have stretch receptors asso- known as the fiber tract, which contains many fibers.
ciated with the fore and hindguts, and these perhaps are These fibers are secreted by the tract cell, which lies
universally present. Large numbers are present on the within the connective tissue and also has a giant nucleus.
foreguts of grasshoppers and crickets where they probably The neuron gives rise to two to four main dendrites,
monitor the movement of food along the gut. In grass- which run along the length of the fiber tract. From these
hoppers, they also monitor foregut distension, regulating main dendrites, side branches, which are not clothed in
meal size (Bernays & Chapman, 1973). Others monitor the glial cells at the tips, are embedded in dense bundles of
amount of food present in the hindgut (Simpson, 1983) fibers (Osborne, 1970). In adult beetles, the neurons of
and probably regulate fecal production. A pair of multi- muscle stretch receptors associated with the mandibles
polar stretch receptors is also present on the bursa copula- indent the muscle membrane, ending near the Z-bands
trix of the cabbage butterfly, Pieris. These receptors (Honomichl, 1978). Muscle receptors have been described
monitor distension of the bursa, which is normally caused in Orthoptera, Neuroptera, Coleoptera, Trichoptera and
by the placement of the spermatophore. This distension Lepidoptera.
causes the female to refuse further matings. Multipolar
receptors, together with chordotonal organs, at the base of Occurrence of strand and muscle receptors Stretch
the ventral gonocoxa of Teleogryllus monitor movement of receptors of these types are probably present in the
the egg during its passage from the oviduct, and perhaps abdomen of all insects. Dorsally, a pair extends from the
regulate the delivery of sperm from the spermatheca tergum to the intersegmental membrane or from one
(Sugawara, 1993). intersegmental membrane to the next. Orthopteroid
Multipolar stretch receptors have also been reported insects and beetles also have a vertical stretch receptor on
on or within the nerves of a variety of insects and are prob- each side of each segment, and some species also have
ably of widespread occurrence. They respond to stretch- ventral stretch receptors. Comparable dorsal receptors are
ing of the nerve which may arise from a variety of causes, present in the thorax of some insects.
depending on the position of the nerve. Elsewhere in the body, strand or muscle receptors are
Review: Finlayson, 1976 associated with the mouthparts, legs and wings. The wing
stretch receptors of locusts play a key role in the control of
23.3.2 Receptors with accessory structures wing movements (section 9.10.3).
Where stretch receptors are not immediately associated
with an epithelium or a nerve, they are usually supported 23.3.3 Functioning of stretch receptors
by a strand of connective tissue or a modified muscle fiber, Stretch receptors have none of the obvious structural fea-
known as strand and muscle receptors, respectively, tures, either within the dendrites, such as the tubular body,
although there appears to be a great variety of forms. or outside them, such as the scolopale, that occur in other
A strand receptor consists of a strand of connective mechanoreceptors. In all cases, however, large numbers of
tissue, extending from one structure to another, with a naked dendritic endings are embedded in connective tissue
multipolar neuron on the outside or embedded within it or in the basal lamina of the tissue with which the receptor
(Fig. 23.20a). The neuron is sheathed in glial cells except is associated. It is inferred that transduction results from
for the tips of the dendrite which are embedded in the con- stretching the membrane of those endings. Although the
nective tissue. Some strand receptors of orthopteroid somata of these cells are usually in the hemocoel, the glial
insects have the soma of the neuron in the central nervous cells surrounding them appear to form an effective
system (Braunig, 1982). ‘blood–brain barrier’ and action potentials result from an
Muscle receptors are associated with a modified inward flow of sodium ions. However, the neurons of
muscle fiber which may be a component of a functional muscle stretch receptors of caterpillars are affected by the
muscle, or may be a separate structure. The fiber contains ionic composition of the medium in which they are bathed
typical muscle fibrils, but these are sparse in the center of (Weevers, 1966a).
632 MECHANORECEPTION
These receptors exhibit tonic activity under sustained during relaxation. It is suggested that this might protect
tension that is proportional to the degree of stretching the receptor from excessive stretch and take up the slack if
(Fig.23.21). In many cases, they also monitor the rate of stretch is suddenly reduced.
stretching, firing faster the higher the rate of stretch. The normal role of these receptors, at least in some
They may also respond to acceleration in the rate of cases, is not simply to monitor changes in position; they
stretching. Because of these characteristics, they have the may also promote negative feedback effects which tend to
capacity to follow low frequency oscillations in the degree restore the system to its initial state. This is most clearly
of stretch. demonstrated in the dorsal muscle stretch receptors of
The role of the muscle in muscle stretch receptors is caterpillars where stretching a muscle receptor organ of
not clear. In caterpillars, the activity of the motor neuron one segment affects the activity of at least 32 different
to the stretch receptor muscle is inhibited when the stretch motor units. These are on the contralateral side of the
receptor is stretched, but exhibits a transient decrease same segment and the ipsilateral side of adjacent segments
during stretching and a transient increase in activity (Weevers, 1966c).
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Menzel, J.G. & Tautz, J. (1994). 5, 77–100. electrophysiological response of the
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Stumpner, A. (1997). An auditory inter- Tautz, J. (1978). Reception of medium Weevers, R. de G. (1966b). The physiol-
neurone tuned to the male song fre- vibrations by thoracic hairs of caterpil- ogy of a Lepidopteran muscle receptor
quency in the duetting bushcricket lars of Barathra brassicae L. I. The sensory response to stretching.
Ancistrura nigrovittata (Orthoptera, (Lepidoptera, Noctuidae). II. Response Journal of Experimental Biology, 44,
Phaneropteridae). Journal of characteristics of the sensory cell. 177–94.
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Sugawara, T. (1981). Fine structure of the 67–77. ogy of a Lepidopteran muscle receptor
stretch receptor in the bursa copulatrix Thorpe, W.H. & Crisp, D.J. (1947). III. The stretch reflex. Journal of
of the butterfly, Pieris rapae crucivora. Studies on plastron respiration. III. Experimental Biology, 45, 229–49.
Cell and Tissue Research, 217, 23–36. The orientation responses of Williamson, R. & Burns, M.D. (1978).
Sugawara, T. (1993). Oviposition behav- Aphelocheirus (Hemiptera, Multiterminal receptors in the locust
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modus: mechanosensory cells in the tion to plastron respiration: together Physiology, 24, 661–6.
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integument of the cricket, Teleogryllus noctuid moths: responses to the search- exoskeleton and insect proprioception.
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Tautz, J. (1977). Reception of medium Weevers, R. de G. (1966a). A forces in the American cockroach,
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Mechanical properties of receptor herbivorous insect. Journal of
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Physiology, 118, 13–31.
24 Chemoreception
Stimulation by chemicals involves the senses of smell data. The pores vary in diameter from 10 to over 25 nm in
(olfaction) and taste (gustation). Olfaction implies the sensilla of different insects and their density varies from
ability to detect compounds in the gaseous state. Taste, in about 5 m⫺2 on the trichoid sensilla of Bombyx to
humans, refers to detection of compounds in solution, or 125 m⫺2 on the plate sensilla of Apis. Within the pore, in
in a liquid state, by receptors in the oral cavity. Insects have many cases, is a circular cavity called the pore kettle from
comparable receptors on many parts of the body, often which fine pore tubules, 10–20 nm in diameter, pass for a
using them for purposes unrelated to feeding, and they short distance into the lumen of the sensillum (Fig. 24.2b).
also have the ability to detect chemicals on dry surfaces as Different types of sensillum may have as many as 50 pore
well as in solution. For these reasons, it is usual to refer to tubules arising from each pore kettle, or as few as five, or
‘contact chemoreception’ in insects rather than ‘taste’. even none at all, although the extent to which these differ-
The distinction between olfaction and contact chemo- ences are artifacts is not certain. These tubules are the
reception is usually clear, although olfactory receptors can remnants of wax canals (section 16.2.3) remaining after the
respond to substances in solution and contact chemo- trichogen cell has withdrawn from the cuticle. They some-
receptors respond to high concentrations of some odors. times appear to extend inwards to make contact with the
Processing within the central nervous system is, however, dendrite, but this is not generally true.
quite different. The axons from all olfactory receptors ter- The gross cuticular form of the sensilla is very variable.
minate in the antennal lobes in the brain (section 20.4.2) They may be relatively long hairs with thick walls often
whereas axons from contact chemoreceptors terminate 0.5 m or more in thickness (trichoid sensilla); short
within the ganglion of the body segment on which the finger-like projections with thin cuticle less than 0.3 m
receptors occur. thick (basiconic pegs); flat plates level with the general
Reviews: Frazier, 1992 – chemoreceptor physiology; Morita & surface of the cuticle (plate or placoid sensilla); or short
Shiraishi, 1985 – chemoreceptor physiology; Payne, Birch & pegs sunk in depressions of the cuticle and opening to the
Kennedy, 1986 – olfaction exterior via a relatively restricting opening (coeloconic
sensilla) (Fig. 24.3a). Amongst the latter, the wall of the
peg is often hollowed out by a series of extensions of the
24.1 OLFACTION peg lumen. These are called double wall pegs and the pores
often arise from longitudinal furrows on the surface (Fig.
24.1.1 Structure of receptors 24.3b). Many variations on these general themes have been
Olfactory sensilla comprise cuticular and cellular compo- described. Olfactory hairs and pegs usually arise from the
nents comparable, in a general sense, to those of cuticular cuticle without any specialized socket region.
mechanoreceptors and contact chemoreceptors (Fig. 24.1, A dendrite sheath surrounds the dendrites within the
and compare Figs. 23.1, 24.8). receptor lymph cavity, but usually ends at the hair base, the
Review: Zacharuk, 1985 dendrites emerging from it.
In some insects, complex olfactory organs are formed
Cuticular components The cuticle of olfactory recep- from the fusion of a number of sensilla. This is common in
tors is characterized by the presence of numerous small Homoptera where the rhinaria of aphids are formed from
pores which permit the entry of chemicals (Figs. 24.1, the fusion of up to six separate units, and the plaque
24.2). These sensilla are called multiporous, and, in most organs of the fulgorid, Pyrops, from as many as 35. Other
cases, their function as olfactory receptors is inferred from compound olfactory sensilla are known from some beetles
this structure since there is relatively little experimental and larval Musca (see Zacharuk, 1985).
[636]
OLFACTION 637
Cellular components The cells of olfactory sensilla are into the lumen of the hair, or close beneath the cuticle of
derived from the epidermis like those of other cuticular pore plates (Fig. 24.1). Consequently, the distal dendrites
sensilla. The number of sensory neurons in olfactory sen- are bathed directly by the receptor lymph. In some cases,
silla varies in different insects. Two are commonly present the distal dendrites branch.
in the thick-walled pheromone-specific sensilla of male The axons from the neurons extend, without synapses,
moths, but over 20 are present in some thin-walled recep- to the antennal lobes, ending in arborizations that form the
tors of grasshoppers. Coeloconic sensilla often have three olfactory glomeruli. It is generally supposed that each
neurons. neuron ends in one glomerulus, and that all neurons
The proximal and ciliary regions of the dendrite are responding to the same compound, or group of com-
similar to comparable regions of mechanoreceptors, but pounds, end in the same glomerulus (section 20.4.2). This
distally the dendrite leaves the dendrite sheath and extends is true for multiporous sensilla on the palps as well as those
638 CHEMORECEPTION
cuticle
1 m
b)
outer layer
of epicuticle
pore canal
pore kettle
cuticle
pore tubule
receptor lymph
100 nm
OLFACTION 639
opening at surface
a) of cuticle
pore
b)
cavity
dendrite
peg
ridges of
cuticle
dendrite
dendrite lumen of
sheath peg
receptor lymph
cavity
tormogen cell
electron dense
cuticle material
Fig. 24.3. Coeloconic sensillum. (a) Longitudinal section showing the peg in a cavity beneath the surface of the cuticle.
(b) Transverse section through a double-walled peg.
on the antennae. In Manduca, there is a single glomerulus Various types of olfactory sensilla are present on the
in each antennal lobe in which the axons from the palp sen- antennae of any insect. For example, three distinct types
silla end. In most cases, the inputs from olfactory receptor are found in grasshoppers, two types of basiconic and one
neurons end in the ipsilateral antennal lobe, but in Diptera of coeloconic sensilla (a second type of coeloconic sensil-
many of the neurons connect with the lobes of both sides. lum responds to temperature and humidity (section 19.7)).
This is also true of the palp receptors in Manduca. In the midge, Culicoides, there are four types, two of tri-
The accessory cells of olfactory sensilla are essentially choid sensilla, one of basiconic and one of coeloconic sen-
similar to those of mechanoreceptors (Fig. 24.1). They silla. These different types are usually associated with
vary in number from two to four, but usually there are neurons responding to different classes of chemical.
three: the thecogen, trichogen and tormogen cells. In addi- Sensilla with the same outward form may contain neurons
tion to their development functions, these cells regulate which respond to different ranges of compounds so that
the composition of the receptor lymph. Pheromone- the number of physiological classes may be considerably
binding protein (see below), is produced continuously by greater than the number of anatomical classes. By contrast,
the trichogen and tormogen cells of antennal sensilla in olfactory sensilla on the palps tend to be structurally
Antheraea. The same two cells, probably together with the uniform.
thecogen cell and the neuron, are also involved in the Reviews: Altner & Prillinger, 1980; Steinbrecht, 1987;
breakdown of the protein (Steinbrecht, Ozaki & Zacharuk, 1985; Zacharuk & Shields, 1991 – distribution on
Ziegelberger, 1992). larvae
Distribution Multiporous, olfactory sensilla are proba- 24.1.2 Functioning of the receptor system
bly present on the antennae of all insects, including most Two processes, which can be regarded as analogous to cou-
larval forms. In addition, some insects may have multipor- pling and transduction in mechanoreceptors, are involved
ous sensilla on the maxillary and labial palps. These may be in producing the neuronal response. The first is the
relatively few in number, as in grasshoppers, or there may capture and transport of odor molecules to the dendrite
be large numbers as on the labial palps of Lepidoptera. membrane, known as perireceptor events. The second is
Multiporous sensilla also occur on the genitalia of the transduction, the conversion of chemical to electrical
sheep blowfly, Lucilia. energy.
640 CHEMORECEPTION
odor binding
protein
receptor
molecule
dendrite
receptor
lymph
Perireceptor events Most odor molecules are to some In this solubilized form, the odor molecules are carried
extent lipophilic, and so they will dissolve in the epicut- to the membrane of the dendrite where, it is assumed, they
icular lipid forming the outer coating of a sensillum (Figs. are released from the binding proteins and become associ-
24.2, 24.4), but they do not readily dissolve in the insect’s ated with receptor proteins.
body fluids. A consequence of the former is that the whole
outer surface of the sensillum is involved in the capture of Transduction Transduction occurs at the dendrite
odor molecules; it is not necessary for the molecules to membrane. It is thought that protein molecules in the
strike the pores directly (Kanaujia & Kaissling, 1985). A outer surface of the cell membrane bind with odor mole-
consequence of the latter is that they must be solubilized in cules. These receptor molecules are believed to be rela-
order to reach the dendritic membrane. This is achieved by tively specific for the type of odor molecule with which
combining with specific water-soluble proteins, called they bind. Work on the olfactory system of some other
odor-binding proteins. Three classes of such proteins have animals suggests that there may be a large family of recep-
been recognized: pheromone-binding proteins and two tor molecules giving the organism the potential of dis-
classes of general odor-binding proteins. The former criminating among a wide range of compounds. A small
usually occur only in male moths where they bind number of possible receptor proteins have been identified
specifically with components of the female sex in insects.
pheromone. General odor-binding proteins are present in Acting via a second messenger system that probably
the olfactory sensilla of both sexes. They are believed to involves inositol trisphosphate, capture of an odor mole-
bind non-specifically with many different classes of odor cule by a receptor molecule produces a depolarization of
molecules (Steinbrecht, Laue & Ziegelberger, 1995). the cell membrane, called a receptor potential. This
These proteins may be at high concentrations in the recep- spreads electrotonically to the soma and leads to the pro-
tor lymph. For example, the pheromone-binding protein duction of action potentials if it is of sufficient magnitude.
of Antheraea is present at a concentration of about 10 mM. However, some odors produce a hyperpolarization of the
OLFACTION 641
pheromone cell plant odor cell Stimulus degradation It is necessary for stimulating
molecules to be removed quickly from the dendrite and the
action potentials (number.s -1)
100 heptanol
sensillum lymph in order to maintain sensitivity, and so
hexanol
that the neural signal is temporally related to the occur-
octanol
rence of the environmental stimulus. Two possible mecha-
50
nisms have been suggested. One is that the odor molecules
are degraded by enzymes. Two types of enzyme are known
heptanal
to occur in the receptor lymph of male Antheraea. An este-
nonanol
rase specifically degrades the acetate component of the
0 female sex pheromone, and an aldehyde oxidase, also
-2 -1 0 1 2 3 4 present in the female, acts on a range of different com-
odor concentration (log) pounds. The odor-binding proteins probably protect the
odor molecules from the enzyme during transit to the den-
Fig. 24.5. Sensitivity of two olfactory neurons of male
drite. However, it is not certain that enzymic degradation
Spodoptera. The pheromone cell is sensitive to a minor
pheromone component, Z9,E12-14 acetate. Notice that its occurs sufficiently rapidly to limit the duration of a stimu-
dynamic range extends over odor concentrations of about two lus. The alternative possibility is that the odor-binding
orders of magnitude. The plant odor cell responds maximally to protein serves, not only to carry the odorant molecules to
heptanol. This cell responds to other related compounds, but less the dendrite, but also to inactivate them. In a reduced form
strongly. Notice that both chain length and functional group are it may act as a carrier becoming oxidized at the receptor
important. Concentration is shown as the amount of each membrane so that the pheromone molecule is no longer
compound in g (log scale) applied to the cartridge which acted available to stimulate (Ziegelberger, 1995). Enzymic
as the source of odor. The concentration at the receptor will be degradation may then follow more slowly.
proportional to this for compounds of similar volatility (after
Because the odor molecules are first trapped at the
Anderson, Hansson & Löfqvist, 1995; Ljungberg, Anderson &
surface of the cuticle, their transport into the sensillum is
Hansson, 1993).
relatively slow. This could provide the insect with false
information about the occurrence of a stimulus, and there
cell membrane, and may act via a different second messen- is some evidence that enzymes degrading odor molecules
ger system involving cAMP. are also present in the cuticle.
Olfactory neurons commonly exhibit a low level of
spontaneous activity, producing action potentials even in Specificity Neurons vary in the specificity of their
the absence of any odor. Consequently an odor may response to odors. Many pheromone receptor neurons are
enhance the level of activity, have no effect, or reduce activ- highly specific, effectively responding only to a single
ity. All these effects may occur in one neuron in response to compound and often showing marked selectivity even for a
different compounds. specific isomer (Fig. 24.6a). Such cells may respond to
The response to a compound that increases the rate of other compounds, but usually only at concentrations
firing is often phasic/tonic and it may continue for a brief several orders of magnitude higher than that of the com-
period after removal of the stimulus. The magnitude of the pound to which they are tuned. There is increasing evi-
response increases with stimulus concentration until the dence that some neurons responding to host-related odors
receptor is saturated (Fig. 24.5). The dynamic range of are also specific. For example, in Spodoptera littoralis 21
neurons usually extends over a concentration range of two classes of neurons have been identified on the basis of the
or three orders of magnitude. At lower concentrations, compounds, other than sex pheromones, that they
below threshold, the neuron does not respond; at higher respond to. Except for those responding to the common
concentrations it normally responds maximally. Threshold green leaf compounds, most of the different classes
concentrations vary considerably. Pheromone-specific respond only to one or two particular compounds. None of
neurons, for example, often have much lower thresholds the cells responds to a wide range of compounds
than neurons responding to other types of odor (Fig. 24.5). (Anderson, Hansson & Löfqvist, 1995; see also Blight et
Reviews: Vogt, 1995; Vogt, Rybczynski & Lerner, 1990 al., 1995).
642 CHEMORECEPTION
3 Ac COOH
4 CHO
CHO COOH CH2 OH
5 Ac
CHO COOH CH2 OH
6 Ac
7 Ac CHO COOH
8 Ac COOH
9 OH O
10 COOH
CHO CH2 OH
11 Ac HOOC
COOH
0 20 40 60
Ac = acetate
action potentials
(number.s -1)
CHO CH2OH O
strongly stimulating
O O
methylhexanone methylheptanone citral nerol β-ionone
OH
OH
weakly stimulating O
OH H CH2OH OCH3
H C OH C
not stimulating O O HO CH 2 CH CH 2
Fig. 24.6. Specificity of olfactory receptor neurons. (a) Specialist neuron on antenna of male Mamestra. This cell responds
primarily to one of the components of the female sex attractant pheromone, Z11-hexadecen acetate (compound 8). Notice
that it shows no response to the E11-isomer (compound 7) or to Z11-hexadecen alcohol (9) or aldehyde (10). Acetates with
different chain lengths, 14 (compounds 1–3) or 17 (11) carbon atoms, produce moderate responses only if the double bond is
in the Z11 position (based on data in Renou & Lucas, 1994). (b) Group specialist neuron in a coeloconic sensillum on the
antenna of Locusta. The cell is sensitive to various forms of hexanoic acid and some related compounds. Degree of shading
indicates intensity of response (darkest ⫽greatest sensitivity). Compounds not in boxes did not stimulate (after Kafka, 1971).
(c) Generalist olfactory neuron in the antenna of Periplaneta. This cell responds primarily to monoterpenes. Notice that nerol
is strongly stimulating (top row), but geraniol, its stereoisomer, does not stimulate (bottom row). The cell responded to more
compounds than those shown in the diagram. Some other cells on the antenna have similar, although not identical, response
spectra, while others are quite different (data from Selzer, 1981).
OLFACTION 643
Other neurons appear to be less specific, responding to Temporal response patterns Airborne odors do not
a range of closely related compounds. Several leaf-feeding form a continuous gradient because of air turbulence;
insects have sensory neurons that respond to a range of instead they occur as a discontinuous series of bursts
commonly occurring six-carbon-atom volatiles from separated by ‘clean’ air. The ability to distinguish succes-
green leaves, such as hexanoic acid (Fig. 24.6b), but not to sive contacts with such odor bursts is important in odor-
other types of compound. Generalist receptors respond to modulated flight and the ability to do so depends on the
a range of structurally different compounds, and cells of characteristics of the sensory neurons.
this type are present in Periplaneta (Fig. 24.6c) and in some Males of the moth, Helicoverpa, have large numbers of
bark beetles. Even here, the neurons are differentially olfactory neurons on the antennae which respond to the
responsive to different compounds (Mustaparta, 1975; principal component of the female sex attractant
Selzer, 1981). pheromone. Some of these exhibit a strong phasic
A neuron’s specificity is assumed to be largely a conse- response which rapidly falls to zero. These neurons give
quence of the receptor molecules present in its dendritic discrete responses to 20 ms pulses of pheromone at 1.5 Hz;
membrane. It is presumed that binding depends on molec- at 6 Hz the response is continuous, but distinct peaks still
ular shape, and that a neuron that responds primarily to a correspond with the arrival of the stimulus. Only at 12 Hz
single compound has only one type of receptor molecule do the responses merge into a continuum from which the
with very specific binding properties. Neurons that insect probably cannot distinguish the pulsed nature of the
respond to a group of related compounds possibly have a stimulus from continuous stimulation. Thus, the periph-
single receptor site with characteristics that enable it to eral neurons have the capacity to allow the insect to recog-
bind with different molecules provided they have some nize a stimulus that is pulsed at quite high frequency
characteristic structure. In this case, some compounds (Almaas, Christensen & Mustaparta, 1991).
presumably have a less good fit with the receptor molecule
and so produce lower firing rates. The plant-odor-specific Odor discrimination It is clear from the behavior of
neuron depicted in Fig. 24.5 is probably of this type. insects that they are able to discriminate between odors.
Neurons that respond to a number of structurally different This is most obvious with respect to pheromones where
compounds may have several different types of receptor closely related species respond to their own pheromones,
molecules binding to structurally different odor mole- but not to those of other species. It is also apparent from
cules. The specificity of the odor-binding proteins may studies showing that bees and other insects can be trained
also be important in determining the types of molecule to distinguish between odors.
that reach the dendrite. Specific odor recognition often depends on the occur-
The sensitivity of the insect as a whole is influenced by rence of sensory neurons responding only to certain com-
the number and arrangement of the sensilla. The greater pounds. This information is relayed to specific glomeruli
the number of sensilla, the more molecules will be cap- in the antennal lobe and from here, projection neurons
tured and the more information sent to the brain. Thus, specific for the odor may extend to other parts of the brain
the males of species in which the female emits a sex attrac- (section 20.4.2). This is called a labelled line system.
tant pheromone often have pectinate antennae with many Labelled line systems are the product of evolved adapta-
branches providing space for a large number of sensilla. In tions to odors of critical and usual importance to the insect
male Manduca, where the flagellum is stouter than in the and are known to exist in the case of some pheromones. An
female, although not pectinate, there are probably 300 000 alternative way of recognizing different odors is by across-
neurons responding to components of the sex attractant fiber patterning. Here, sensory neurons, or projection
pheromone, and another 100 000 which respond to plant neurons from the antennal lobe, respond to a range of
odors. Females have only this latter class of neurons with compounds, but cells differ in their relative sensitivity to
which to locate their host plants for nectar feeding and particular chemicals. The information carried by a single
oviposition. It is believed that the difference in number is a projection neuron does not convey a clear message, but the
reflection of the very low concentrations of pheromone patterns of response of all the neurons together may be
emitted by females compared with the concentration of sufficiently distinct for the insect to distinguish between
plant odors. odors.
644 CHEMORECEPTION
may also affect behavior close to the source, and responses are stimulated to land on artificial leaves by the odor of
to odors may be learned. carrot leaves, the normal host plant of the larvae, but this
Because of air turbulence, continuous odor gradients behavior is disrupted if the odor of cabbage is also present.
cannot persist under natural conditions except for very Examples of insects being repelled by odors are also
short distances. Consequently, although odor may provide known. For example, nepetalactone, the chemical giving a
the signal that initiates upwind flight, the insect depends characteristic odor to catnip, repels a number of phy-
on a combination of mechanical and visual stimuli to tophagous Homoptera and Coleoptera (Eisner, 1964) and
achieve upwind movement. This type of behavior is linalool is a repellent for the aphid Cavariella.
known to occur in response to sex attractant pheromones, Reviews: Bernays & Chapman, 1994 – behavior in relation to
such as those produced by many female Lepidoptera. It host-plant odors; Colvin & Gibson, 1992 – host-finding by tsetse
may also occur in relation to food, or an oviposition site flies; Murlis, Elkinton & Cardé, 1992 – odor plumes; Payne,
especially in night-flying insects where a direct visual Birch & Kennedy, 1986 – physiology and behavior; Visser, 1986 –
response may only be possible close to the source. odor perception in phytophagous insects
Although single compounds can sometimes induce
these behaviors, it is probably generally true that specific- 24.2 CONTACT CHEMORECEPTION
ity of attraction, where it occurs, results from particular
combinations of compounds. For example, although a 24.2.1 Structure of receptors
single compound can attract males to a pheromone-pro-
ducing female, a mixture of two or three specific com- Cuticular components Contact chemoreceptors are
pounds provides the insect with an unambiguous signal usually short hairs or cones characterized by the presence
(see Chapter 27). Similarly, a specific mixture of the com- of a single pore at, or close to, the tip of the projection (Fig.
monly occurring six-carbon-atom green leaf volatiles is an 24.8). Sensilla having this structure, but whose function
attractant for the Colorado potato beetle, Leptinotarsa, and has not been experimentally investigated are often called
many insects have olfactory neurons responding to these uniporous sensilla; the assumption is that they are contact
compounds. Sheep blowflies are attracted to injured sheep chemoreceptors. The pore may be circular or oval to slit-
by the sulfur-containing breakdown products of wool. shaped, and is often about 0.2 m in longest diameter. At
Dimethyldisulfide and ethanediol, together with hydrogen least in some instances, a porous plug within the pore
sulfide are major components of this odor, but, individu- separates the dendrite endings from the environment. The
ally, neither dimethyldisulfide nor ethanediol has any effect plug appears to be composed of fibrils of cuticular material
on the fly’s behavior (Ashworth & Wall, 1994). (Shields, 1994). The dendrite sheath extends inwards from
Carbon dioxide is an attractant for many species that the inner edge of the pore and appears to be continuous
suck vertebrate blood and there are carbon dioxide recep- with the epicuticle. In the contact chemosensory hairs of
tors on the antennae of tsetse flies (Bognor, 1992), and pre- grasshoppers the dendrite sheath lies in the center of the
sumably of other blood-sucking species. The carbon hair surrounded by the receptor lymph which extends into
dioxide acts, together with acetone, octenol and other com- the hair. In flies, however, the lumen of the hair is divided
pounds commonly occurring in animal breath, to attract into a smaller lateral compartment containing the den-
tsetse flies. Interestingly, many Lepidoptera have large drites and a larger one occupying most of the space within
numbers of carbon dioxide receptors in a pit on the labial the hair. The dendrite sheath in this type is continuous
palps. In Heliothis, these are sensitive to very small changes with the walls of the lateral compartment.
in the ambient level of carbon dioxide, although their role Hair-like sensilla usually have sockets similar to those
in the behavior of the insect is not known (Stange, 1992). of mechanoreceptor hairs giving them some mobility.
There are relatively few examples of odor affecting Cone-shaped sensilla are found primarily on the inner
behavior at close range even though such behavior may be mouthparts. They lack an articulation, the cone being
widespread. Flower scents on the bodies of bees returning continuous with the surrounding cuticle.
from foraging help other workers recognize the food
source. Male monarch butterflies produce an aphrodisiac Cellular components The neurons of contact chemo-
pheromone which enhances the female’s readiness to mate. receptors are essentially the same as those of olfactory
Females of the black swallowtail butterfly, Papilio polyxenes receptors except that their dendrites extend to the tip of
646 CHEMORECEPTION
the hair or cone within the dendrite sheath (Fig. 24.8). a dry surface, like the surface of a leaf or, in the case of
There are commonly four chemosensitive neurons in a contact pheromones, a member of the opposite sex. It is
sensillum, but some sensilla have larger numbers. In addi- likely that compounds in the viscous fluid at the tip of the
tion, socketed sensilla have a mechanosensitive neuron hair function as carriers for some compounds on these sur-
which ends at the cuticle of the hair base and has a tubular faces. In sensilla on the palps of Periplaneta, a sugar-
body at the point of insertion. binding protein is present within this material (Becker &
The tips of the chemoreceptor dendrites are covered by Peters, 1989) and a protein in the same family of proteins
a viscous fluid containing mucopolysaccharide which as pheromone-binding protein in olfactory sensilla
sometimes exudes through the terminal pore of the sensil- (section 24.1.2) is present in contact chemoreceptors on
lum. the proboscis and tarsi of flies (Ozaki et al., 1995). The
The axons terminate in the ganglion of the segment on mucopolysaccharide possibly also functions as a filter as
which the receptor occurs. Thus, the input from sensilla not all substances will be equally readily transported.
on the maxillae and labium end in arborizations in the sub- Transduction mechanisms probably vary depending
esophageal ganglion, and those from sensilla on the legs on the type of compound to which the neuron responds,
end in the thoracic ganglia. but almost nothing is known of the processes in insects. By
Two or three accessory cells are present in each sensil- analogy with vertebrates (see Avenet, Kinnamon & Roper,
lum, with similar functions to those of mechano- and 1993), it may be that inorganic ions act directly on ion
olfactory receptors. channels in the dendritic membrane, whereas there are
protein receptor molecules in the membrane for other
Distribution Contact chemoreceptors may be present types of chemical. Two proteins which probably serve this
on all parts of the body, although major concentrations function are present in the sugar receptors of the fly,
occur on the labrum, maxillae and labium (see Fig. 2.6). Phormia (Ozaki et al., 1993) (see below). Binding of the
Moderate numbers occur on the antennae, especially at the ligand to these receptors probably initiates a second mes-
tip. Chemoreceptors are not present on the mandibles. Nor senger cascade leading to an alteration of the membrane
do they occur within the gut1, although many, perhaps all, permeability to produce the receptor potential.
insects have chemoreceptors in the wall of the cibarium. The receptor potential is presumed to develop distally
Relatively large numbers of receptors are often present on on the dendrite and then to spread passively to the spike
the legs, but, although contact chemoreception may be (action potential) initiation zone, possibly at the origin of
important in oviposition, only a few, and sometimes none the axon from the soma. The magnitude of the receptor
at all, are present on the ovipositor. In addition to those potential is proportional to the concentration of stimulat-
associated with specific organs, grasshoppers have large ing compound and as the number of action potentials pro-
numbers of small trichoid contact chemoreceptors scat- duced is proportional to the size of the receptor potential,
tered over all parts of the body. Stocker (1994) gives a com- there is a direct relationship between concentration and the
plete compendium of the chemoreceptors of adult number of action potentials. Hyperpolarization decreases
Drosophila. the likelihood that action potentials will be produced.
Review: Zacharuk & Shields, 1991 – distribution in larvae The dynamic range of contact chemoreceptor neurons
extends over concentration ranges of two or three orders of
24.2.2 Functioning of contact chemoreceptors magnitude, similar to that of olfactory receptors.
Very little is known about the physiology of contact Threshold levels differ between neurons. Cells responding
chemoreception. The receptors on the inner parts of the to major nutrient compounds, such as sugars and amino
mouthparts are probably, during feeding, bathed by saliva acids, are usually sensitive only to moderately high
and fluids released from the food and so respond to chem- concentrations (Fig. 24.9a, b), but cells responding to
icals in solution. Sensilla of the tarsi and other parts of the chemicals with specific ecological relevance apart from
body, however, probably normally respond to chemicals on nutrition are often much more sensitive (Fig. 24.9c, d).
1 Receptors involved in the transport of some nutrients from the gut Even within a single insect, neurons responding to the
lumen into the midgut cells probably are present, but these have same compound may have different thresholds. For
only a local effect; they are not connected with the nervous system. example, in Phormia, the neurons in the tarsal hairs that
CONTACT CHEMORECEPTION 647
a) opening at
parts tip of hair
of neuron b)
hair viscous fluid
porous plug
distal dendrites
extending to tip of distal
hair dendrites
socket
wall of
hair
cuticle
dendrite
sheath
receptor lymph
cavity
epidermal cell
trichogen c)
cell
dendrite
ciliary region sheath
of dendrites tormogen
cell
dendrite
proximal
dendrites thecogen
cell
somata
basal lamina
axons
Fig. 24.8. Contact chemoreceptor. (a) Longitudinal section showing general structure. (b) Longitudinal section of tip
showing detail of structure. (c) Transverse section through the dendrite sheath and distal dendrites in the receptor lymph
cavity.
respond to sucrose have thresholds at concentrations one When a grasshopper, for example, drums on a leaf with its
or two orders of magnitude lower than those in labellar palps (palpates) the contact chemoreceptors on the tips of
sensilla (Fig. 24.10). Such differences provide the insect the palps touch the surface about 10 times a second, each
with a greater dynamic range of response than can occur in contact lasting less than 20 ms. In the intervals between
individual neurons. contact, the neurons disadapt and thus maintain a high
Most contact chemoreceptors exhibit a marked phasic level of input for a second or more.
response often with only a short-lived tonic response Unlike olfactory neurons, contact chemoreceptor
during continuous stimulation. As a consequence, the neurons generally fire only when stimulated, but if they do
input from a single neuron may fall to zero very quickly, exhibit spontaneous activity, the firing rate is very low.
sometimes in less than one second. Perhaps to maintain a
flow of sensory information, many insects make drum- Specificity Each of the neurons within a sensillum
ming movements with the legs, palps or antennae in which responds to a different class of compound. It is common
they touch a surface repeatedly for very brief periods. for one cell to respond primarily to inorganic salts and
648 CHEMORECEPTION
sucrose
100
sinigrin
glucose
50
no response to:
xylose
fructose
inositol
0
proline response to
strychnine in
100 medial sensillum
histidine
asparagine
chlorogenic acid
phenylalanine
50
no response to: cyanin chloride
methionine arginine no response to
aspartic acid strychnine in
lateral sensillum
glutamic acid
0
10 -7 10 -5 10 -3 10 -1 10 -7 10 -5 10 -3 10 -1
concentration (M) concentration (M)
Fig. 24.9. Responses of the four cells in the lateral styloconic sensillum of the caterpillar of Pieris brassicae. The activity of
each cell is shown during the first second of stimulation. The position of the sensillum is shown in Fig. 2.6b. (a) Response of
sugar cell. This cell only responds to sucrose and glucose (after Ma, 1972). (b) The amino acid cell responds to 14 out of 22
amino acids tested (after van Loon & van Eeuwijk, 1989). (c) Response of the glucosinolate cell to sinigrin. This cell responds
to many glucosinolates. Notice the very low threshold. The cell starts to respond at a concentration of 2 ⫻10⫺7 M sinigrin
(after Blom, 1978). (d) Response of the deterrent cell. This cell responds to a number of phenolic acids and flavonoids. It does
not respond to strychnine, but a deterrent cell in the medial styloconic sensillum is very sensitive to this compound with a
very low threshold (after Blom, 1978; van Loon, 1990).
another to sugars (Fig. 24.9a). The other neurons within a Glucosinolates are characteristic compounds of
sensillum are also relatively specific, although the com- Brassicaceae. Both sexes of adult fruit flies, Rhagoletis, in
pounds to which they respond vary from species to species which the female marks fruit with a pheromone after
and from sensillum to sensillum within a species. Amongst oviposition, have neurons in tarsal receptors that are
flies, one cell may respond to water and, in Phormia, to specific for the compound (Städler et al., 1994). In species
very dilute salt solutions. Cells responding to amino acids using contact pheromones in their surface waxes, like
are present in some sensilla of caterpillars and chrysomelid houseflies, there are probably neurons that respond
beetles, and probably in many other insects (Fig. 24.9b). specifically to the compounds in some tarsal sensilla (Wall
There is no evidence that insects can taste proteins. & Langley, 1993).
Some species have chemoreceptor neurons that only Caterpillars and grasshoppers have a cell in some sen-
respond to specific chemicals that are key components of silla that responds to chemicals from a number of different
the food, or to contact pheromones. For example, many chemical classes that produce aversive behavior (see
larval and adult brassica-feeding insects have a cell that Peterson et al., 1993). No cell with an obvious link to aver-
responds to glucosinolates (Fig. 24.9c; Städler et al., 1995). sive behavior has been described in Coleoptera or Diptera.
CONTACT CHEMORECEPTION 649
100
(Dethier & Bowdan, 1989). A similar effect is observed
in insects which do have deterrent cells, such as the
no additives
caterpillars and grasshoppers. Here, as the alkaloid
50 diet with salicin concentration is increased, the responses of the sugar
diet with inositol cells decrease until they are finally silenced completely.
This effect is not restricted to alkaloids or to deterrent
0
compounds; interactions involving many different com-
pounds occur. For example, in Stomoxys, the activity of
neurons responding to inorganic salts in the labellar
c) temporal variation hairs is inhibited by adenine nucleotides for which they
action potentials (number.s -1)
Fig. 24.12. Peripheral inhibition of contact chemoreceptors. (a) Inhibition by quinine (an alkaloid) of the activity of the cell
responding to sucrose in a tarsal sensillum of Phormia (data from Dethier & Bowdan, 1989). (b) Inhibition of a deterrent cell
response to sinigrin by inositol and sucrose in the medial styloconic sensillum of the caterpillar of Trichoplusia. Notice that, in
this insect, sinigrin produces an aversive response and stimulates the deterrent cell [in Pieris, it is a phagostimulant and
stimulates a specific glucosinolate-sensitive cell (Fig. 24.9c)](after Shields & Mitchell, 1995). (c) Mutual inhibition by sucrose
and azadirachtin (a terpenoid which stimulates the deterrent cell). The left-hand column of each pair shows the response to
the single compounds; the right-hand columns show the response of the same cells when sucrose and azadirachtin are mixed
together. Each compound is at the same concentration in the mixture as when presented singly. Neurons in a tarsal sensillum
of adult Helicoverpa (data from Blaney & Simmonds, 1990).
652 CHEMORECEPTION
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Murlis, J., Elkinton, J.S. & Cardé, R. van Wetenschappen – Amsterdam C, 72, receptor for the host marking
(1992). Odor plumes and how insects 491–8. pheromone of the cherry fruit fly,
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Entomology, 37, 505–32. caterpillar eat? The sensory code and synthetic compounds. Physiological
Mustaparta, H. (1975). Responses of underlying feeding behavior. In Entomology, 19, 139–51.
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Physiology, 97, 271–90. New York: Springer-Verlag. cosinolates and cardenolides mediating
Omand, E. & Dethier, V.G. (1969). An Schoonhoven, L.M., Simmonds, M.S.J. oviposition in Pieris rapae. Physiological
electrophysiological analysis of the & Blaney, W.M. (1991). Changes in the Entomology, 20, 175–87.
action of carbohydrates in the sugar responsiveness of the maxillary stylo- Stange, G. (1992). High resolution
receptor of the blowfly. Proceedings of conic sensilla of Spodoptera littoralis to measurement of atmospheric carbon
the National Academy of Sciences of the inositol and sinigrin correlate with dioxide concentration by changes in the
United States of America, 62, 136–43. feeding behaviour during the final labial palp organ of the moth Heliothis
Ozaki, M., Amakawa, T., Ozaki, K. & larval stadium. Journal of Insect armigera (Lepidoptera: Noctuidae).
Tokunaga, F. (1993). Putative taste Physiology, 37, 261–8. Journal of Comparative Physiology A,
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K. & Tokunaga, F. (1995). A putative 144, 509–19. Rezeptorfortsätze und reizleitender
lipophilic stimulant carrier protein Shields, V.D.C. (1994). Ultrastructure of Apparat. Zeitschrift für Zellforschung
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pheromone-binding protein super- (Lepidoptera: Noctuidae). Canadian
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654 CHEMORECEPTION
Steinbrecht, R.A. (1980). Cryofixation Todd, J.L., Haynes, K.F. & Baker, T.C. Vogt, R.G., Rybczynski, R. & Lerner,
without cryoprotectants, freeze sub- (1992). Antennal neurones specific for M.R. (1990). The biochemistry of
stitution and freeze etching of an insect redundant pheromone components in odorant reception and transduction. In
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Ziegelberger, G. (1995). van Loon, J.J.A. (1990). Chemoreception Olfactory sensitivity of gomphocerine
Immunolocalization of pheromone- of phenolic acids and flavonoids in grasshoppers to the odours of host and
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Cell and Tissue Research, 282, 203–17. van Loon, J.J.A. & van Eeuwijk, F.A. silla. In Comprehensive Insect
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Ziegelberger, G. (1992). in larvae of two species of Pieris. Pharmacology, vol. 6, ed. G.A. Kerkut
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pheromone-binding protein in moth Visser, J.H. (1986). Host odor perception Pergamon Press.
antennae. Cell and Tissue Research, 270, in phytophagous insects. Annual Zacharuk, R.Y. & Shields, V.D. (1991).
287–302. Review of Entomology, 31, 121–44. Sensilla of immature insects. Annual
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the chemosensory system in Drosophila moth olfaction: a model for cellular Ziegelberger, G. (1995). Redox-shift of
melanogaster: a review. Cell and Tissue identity and temporal assembly of the the pheromone-binding protein in the
Research, 275, 3–26. nervous system. In Molecular Model silkmoth Antheraea polyphemus.
Systems in the Lepidoptera, ed. M.R. European Journal of Biochemistry, 232,
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Cambridge: Cambridge University
Press.
PART V
Communication
[657]
658 VISUAL SIGNALS: COLOR AND LIGHT PRODUCTION
a) b)
consists of a flat basal plate carrying a large number of
reflected light vertical vanes running parallel with the length of the scale
reflected light
incident light
(Fig. 25.3a). Each vane is supported by a series of vertical
and obliquely horizontal mullions (thickenings).
Collectively, the horizontal mullions of adjacent vanes
1 1 form a series of reflecting surfaces which are spaced such
that a blue color is produced by interference. Similar
2 2 effects are produced by a variety of scale modifications in
different blue and green butterflies (Ghiradella, 1989).
3 3
Interference colors in other insects are produced by
4 4 reflection at the interfaces of layers in the cuticle which
differ in refractive index. The refractive indices of the
Fig. 25.2. Interference colors. Diagrammatic representation alternating layers in the pupa of the danaid butterfly,
of the production of color. At each of the reflecting surfaces Euploea, are 1.58 and 1.37. In jewel beetles (Buprestidae)
(numbered 1–4), some light is reflected while the remainder and tiger beetles (Cicindellidae), these layers are in the
is transmitted at lower intensity, as indicated by the reduced
exocuticle, but in tortoise beetles (Cassidinae) and some
amplitude. Two wavelengths are shown, differing in their
butterfly pupae they are in the endocuticle.
relationship to the spacing between the surfaces (after Richards,
1951). (a) Spacing between reflecting surfaces is half the
In some scarab beetles, the reflecting surfaces are layers
wavelength of the incident light. Reflections from the surfaces of chitin/protein microfibrils with a common orientation
reinforce each other so that a strong reflection of this wavelength in the transparent exocuticle. Because their orientation
occurs. (b) Wavelength of the incident light bears no simple changes progressively in successive layers, forming a helix
relationship to the spacing between surfaces. Light reflected at (section 16.2.1.1), any given orientation recurs at intervals
successive surfaces is out of phase; interference occurs so that and, if the intervals are within the range of wavelengths of
reflection of this wavelength is reduced or eliminated. Since, for light, interference colors are produced. The light reflected
any given spacing between the reflecting layers, most reflected by microfibrils oriented in one direction is polarized, but
wavelengths are out of phase, the reflected light will consist only because the orientation changes with depth in the cuticle,
of those wavelengths depicted in (a).
the plane of polarization also changes.
Whatever the nature or position of the reflecting sur-
which are deeper in the epidermis. Similar granules are faces, the wavelength of the reflected light depends on
present in the epidermis of the grasshopper, Kosciuscola, their spacing. Viewing the surface from a more oblique
which is blue during the daytime (see below). In this angle is equivalent to increasing the distance between suc-
insect, the small granules are about 170 nm in diameter, cessive surfaces so that the color changes in a definite
and the larger ones about 1 m. sequence (known as Newton’s series) as the angle of
viewing is altered. A change in color with the angle of
25.2.2 Interference viewing is called iridescence and is a characteristic of inter-
Interference colors result from the reflection of light from ference colors.
a series of superimposed surfaces separated by distances A constant spacing between the reflecting surfaces
comparable with the wavelengths of light. As a result of produces relatively pure colors, as in the scales of
this spacing, some wavelengths reflected from successive Morpho. Spectral purity is enhanced when the reflecting
surfaces are in phase and are therefore reinforced, while layers are backed by a layer of black pigment which
others are out of phase and are cancelled out (Fig. 25.2). absorbs any transmitted light. By contrast, impure colors
The net result is that only certain wavelengths are reflected are produced if the spacing changes systematically with
and the surface appears colored. increasing distance from the surface of the cuticle. For
Interference colors are common in adult Lepidoptera example, in the pupa of Euploea, the thickness of the
where the layers producing interference are formed by paired layers changes systematically through the depth of
modifications of the scales. Each of the scales of the the endocuticle (Fig. 25.3b). This produces interference
Morpho butterfly which produce its bright blue color over a wide range of wavelengths and the pupae appear
PHYSICAL COLORS 659
Fig. 25.3. Interference color production in different insects. (a) Morpho wing scale. Left: whole scale showing vanes running
parallel with long axis; Right: cross-section of part of scale. The horizontal mullions lie parallel with each other with a regular
spacing of 185 nm. The array of mullions across the scale forms a series of reflecting surfaces which reflect blue light. Notice
that the supporting columns are irregularly arranged so only some are in the plane of the section (based on Smith, 1970). (b)
Euploea pupal cuticle. Left: variation in the thickness of the alternating layers of high and low refractive index in the cuticle.
The paired layers begin (layer 1) about 10 m below the surface of the cuticle. Right: reflectance of light of different
wavelengths from the abdominal sclerites. This produces a metallic golden color as seen by the human eye (based on
Steinbrecht et al., 1985).
golden to human eyes (Steinbrecht et al., 1985). Bronze the different refractive indices of the paired cuticular
and silver interference colors are produced in the same layers compared with the air/cuticle interfaces in
way. Morpho.
The wavelength produced by interference also The brightness of the reflected color increases with the
depends on the refractive indices of the materials number of reflecting surfaces. In Morpho species, there are
forming the layers. The horizontal mullions on Morpho only eight to 12 horizontal mullions, and similar numbers
wing scales are uniformly about 185 nm apart, producing of layers are present in the cuticles of buprestid beetles.
a blue interference color. The paired layers in the exocuti- Only a small percentage of light, less than 40%, is
cle of the scarab beetle, Heterorrhina, are of similar thick- reflected. By contrast, the metallic gold or silver cuticles of
ness, but the interference color produced is green due to pupae of danaid butterflies have over 200 reflecting layers
660 VISUAL SIGNALS: COLOR AND LIGHT PRODUCTION
and almost 80% of the incident light over a broad band of are absorbed depends on the molecular structure of the
wavelengths is reflected (Fig. 25.3b). Amongst scarab compound. Particularly important in the production of
beetles, reflectivity is enhanced by large amounts of uric color are the number and arrangement of double bonds,
acid in the reflecting layers. C苷C, C苷O, C苷N and N苷N. Particular functional
Apart from colors of the human visible spectrum, groups are also important. The ⫺NH2 and ⫺Cl radicals,
ultraviolet is also produced as an interference color. This for example, shift the absorptive region of a compound so
occurs in the white butterflies, Pieridae. In Eurema, for that it tends to absorb longer wavelengths. The color-pro-
example, certain scales possess reflecting lamellae about 55 ducing molecule, known as a chromophore, is often conju-
nm thick separated by air gaps of about 80 nm. This gated with a protein molecule, forming a chromoprotein.
system reflects light with a peak wavelength of 350 nm. Insects are able to synthesize most of their pigments,
Interference is responsible for the iridescence of the but not flavonoids or carotenoids which are, consequently,
membranous wings of many different insects. acquired in the diet. The sources of some other pigments,
found only in a few insects, are unknown.
25.2.3 Diffraction Review: Kayser, 1985
When a ray of light strikes the edge of a groove or ridge,
different wavelengths are bent to varying degrees and 25.3.1 Pigments that are synthesized
white light is split into its component spectral colors. If
there is a series of parallel grooves or ridges, separated by Brown and black of cuticle The black or brown of hard-
about the wavelength of light, the wavelengths reflected ened cuticle often results from sclerotization. Quinone
from each line interfere with each other. In a particular tanning produces dark cuticle, but -sclerotization does
direction, light of a given wavelength is reinforced, while not (section 16.5.3). However, cuticular hardening and
other wavelengths are cancelled out. The conserved wave- darkening are not necessarily tightly linked. This is illus-
length varies with the direction in which the light is trated by albino strains of the locust, Schistocerca, which
reflected. This is known as diffraction and a series of have a hard, but colorless cuticle.
grooves or ridges producing such an effect is called a Dark cuticle is also attributed to the presence of the
diffraction grating. pigment melanin, a nitrogen-containing compound which
Diffraction is responsible for the iridescence of some has been demonstrated in the cuticles of Blattodea,
beetles. It occurs in at least eight beetle families most of Diptera, adult and some larval Lepidoptera, and in
which have diffraction gratings on the elytra, but they are Coleoptera. It is typically present as granules in the exocu-
on the abdomen of Staphylinidae where the elytra are ticle. Insect melanin is a polymer of indole derivatives of
short. The spacings between the lines of the gratings vary tyrosine. Like sclerotization, melanization involves the
from 0.8 to 3.3 m. Scarabaeidae have rows of microtri- production of DOPA and dopaquinone (Fig. 25.4).
chia along the gratings and their effect is to make the Black pigments in the pupal cuticle of some Lepidoptera
insects iridescent when viewed from one direction, but not are not granular, and they are probably not melanin.
from the opposite direction. The rib spacing of some lepi-
dopteran scales is appropriate to produce diffraction Pterins Pterins are nitrogen-containing compounds, all
colors, but their irregularity produces an overlap of spectra having the same basic structure, but differing in the radi-
and so white light results. Diffraction colors are not pro- cals attached to this nucleus (Fig. 25.5). They are syn-
duced in dim light and beetles which iridesce due to thesized from the purine guanosine triphosphate. Not all
diffraction in bright light look black or brown at low light pterins appear colored. Some are important metabolically
intensities. as cofactors of enzymes concerned in growth and
differentiation and may act as controlling agents in these
processes. They often occur together with pigments of
25.3 PIGMENTARY COLORS
another group, the ommochromes, because they are cofac-
Pigments appear colored because they reflect certain wave- tors of the enzymes involved in ommochrome synthesis.
lengths of light; the remainder are absorbed and their The vitamin folic acid also contains a pterin.
energy is dissipated as heat. Which particular wavelengths As pigments, they are colored white (for example,
PIGMENTARY COLORS 661
OH
C C COOH
HO tyrosine N
NH2 N
pterin
H2 N
N N
HO C C COOH
dihydroxyphenylalanine
HO (dopa) OH
NH2
N
N OH
sclerotization xanthopterin
H2 N
O C C COOH N N
O dopaquinone
NH2
OH
N
O C N OH erythropterin
O C COOH
dopachrome H2 N C C COOH
N N N
H OH
OH OH
HO C OH HO pterorhodin
5,6 - dihydroxyindole N N
HO C N N
N
H H2 N NH2
N N C N N
H
O C
indole - 5,6 - quinone Fig. 25.5. Pterins. Pterin is the basic structure from which other
O C
N pterins are derived. Xanthopterin is a yellow pigment present in
H
many insect orders. Erythropterin is a red pigment found in
Hemiptera and Lepidoptera. Pterorhodin is a red pigment
polymerizes occurring in some Lepidoptera. Notice that the pterorhodin
to molecule is essentially two xanthopterin molecules, one a mirror
melanin
image of the other.
a) porphyrin a) anthraquinone
OH OH
CH3 O OH
HOOC OH
NH N
O
HO OH CH2 OH
N HN O OH
b) aphin
CH2 OH
b) bilin
O
HO O OH CH3
N O
N N N OH OH
H
HO CH3
Fig. 25.7. Tetrapyrroles: (a) porphyrin skeleton; (b) bilin
O
skeleton.
Fig. 25.8. Quinone pigments: (a) an anthraquinone, carminic
acid, from Dactylopius cacti; (b) an aphin, neriaphin, from Aphis
Only a few insects, usually living in conditions subject
nerei.
to low oxygen tensions, contain hemoglobin and these are
colored red by the pigment showing through the integu-
ment. In Chironomus (Diptera) larvae the hemoglobin is in Quinone pigments The quinone pigments of insects
solution in the blood, while in the larva of Gasterophilus fall into two categories: anthraquinones and aphins (Fig.
(Diptera) it is in hemoglobin cells. Hemoglobin serves a 25.8). Both occur as pigments only amongst Homoptera,
respiratory function, but perhaps also serves as a protein the former in coccids (Coccoidea), and the latter in
store, and enables the aquatic hemipteran, Anisops, to aphids. Their origins in the insects are not known. They
regulate its buoyancy (section 17.9). may be derived from plants, synthesized by the symbi-
The bilins are usually associated with proteins to otic organisms that are always present in these insects, or,
form blue chromoproteins. Biliverdin occurs in many perhaps, manufactured by the insects themselves.
hemimetabolous insects, but is also found in Neuroptera Anthraquinones are widespread in plants, and some
and some Lepidoptera although the latter usually beetles sequester them, although they do not form pig-
contain other types of bilins. Associated with a yellow ments in these insects. Aphins are known only from
carotenoid, these pigments are responsible for the aphids.
greens of many insects. Sometimes the pigments them- Anthraquinones are formed from the condensation of
selves are green. In Chironomus, bilins derived from the three benzene rings. In the coccids they give the tissues a
hemoglobin of the larva accumulate in the fat of the red, or sometimes yellow, coloration. The best known is
adult and impart a green color to the newly emerged fly. cochineal from Dactylopius cacti. The purified pigment is
In Rhodnius, the pericardial cells become green due to called carminic acid (Fig. 25.8a). It is present in globules in
the accumulation of bilins derived from ingested hemo- the eggs and fat body of the female, constituting up to 50%
globin. of the body weight. The larva contains relatively little
pigment.
Papiliochromes Papiliochromes are yellow and Aphins are quinone pigments formed from the
red/brown pigments known only from the swallowtail condensation of three, in the monomeric forms, or seven
butterflies, Papilionidae. Papiliochrome II is pale yellow benzene rings, in dimeric forms. They are found in the
and is formed from one molecule of kynurenine, derived blood of aphids, sometimes in high concentration, and
from tryptophan, and one molecule of -alanine (Ishizaki impart a purple or black color to the whole insect.
& Umebachi, 1990). Neriaphin is a monomeric form (Fig. 25.8b).
664 VISUAL SIGNALS: COLOR AND LIGHT PRODUCTION
a) β-carotene
HO
Note:
* Darkening may result from sclerotization.
COLOR CHANGE 667
a) organizing centers enhanced by light. Here, the epidermal cells are to some
extent independent effectors, responding directly to
stimulation. This is true of the change from black to blue
in the damselfly Austrolestes, but the reverse change is con-
trolled by a secretion released from the terminal abdomi-
nal ganglion (Veron, 1973).
The significance of these changes is unknown, but they
may be thermoregulatory. Dark insects absorb more radia-
tion than pale ones so they may warm up more rapidly in
the mornings and become active earlier than would be the
b) symmetry systems border symmetry case if they remained pale.
system
other
ommochromes melanin
dopamine morphogen(s)
xanthommatin quinone ? diffusing through
epidermis
3-OHkynurenine dopamine
dopa epidermis
tryptophan tyrosine
scale-forming
cell
3-hydroxykynurenine
dopa tyrosine
tryptophan
hemolymph
3-hydroxykynurenine
dopa
fat body
tryptophan tyrosine
Fig. 25.12. Color patterning in Lepidoptera. Each scale-forming cell has the genetic capacity to form any of the pigments. In
general, each scale only produces one pigment, probably in response to gradients of one or more morphogens. The complete
process can be carried out by the cells, although some precursors, synthesized in the fat body, may also be taken up. The large
horizontal arrows in the epidermis represent different morphogens (based on Koch, 1991).
These changes are controlled by changes in hormone sclerotization, probably also regulates darkening occur-
levels associated with molting and sexual maturation, ring immediately after ecdysis.
but the effects may be very different in different species.
The changes in larval Cerura are initiated by a low level 25.5.2.2 Homochromy
of ecdysteroid in the hemolymph leading to the metabo- The colors of many insects change to match the pre-
lism of 3-hydroxykynurenine to an ommochrome. dominant color of the background. This phenomenon is
Perhaps the commitment peak which occurs before called homochromy. The changes may involve the basic
pupation is normally responsible for the change (section color of the insect or may involve a general darkening. For
15.4.2). Juvenile hormone leads to the accumulation of example, larvae of the grasshopper, Gastrimargus, tend to
xanthommatin in Bombyx caterpillars, but prevents it in assume a color more or less matching the background
Manduca (Sawada et al., 1990). Juvenile hormone, con- when reared throughout their lives on that background
cerned in sexual maturation in adult Schistocerca (section (Fig. 25.15). Insects reared on black become black, those
13.2.4.2), also regulates the accumulation of carotenoids reared on white are pale grey. On a green background,
which make the insects yellow as they become sexually however, most insects develop a yellowish coloration. The
mature. The hormone bursicon, which controls differences are produced by different amounts of black
COLOR CHANGE 669
large
granules
red white
4
yellow
pterin (µg.mg-1)
Fig. 25.14. Ontogenetic changes in pigmentation in Dysdercus nigrofasciatus. Underside of the abdomen of second and fourth
instar larvae and adult male. The change from red to yellow is accompanied by a reduction in the relative amount of
erythropterin present (expressed as g of pterin per mg body weight). The white areas are due to uric acid in the epidermal
cells (data from Melber & Schmidt, 1994).
670 VISUAL SIGNALS: COLOR AND LIGHT PRODUCTION
% in class
rearing from the first stage in
50
containers with different colored
backgrounds (after Rowell, 1970).
25
0 0
75
% in class
50
25
75
% in class
50
25
insect colors
pigment, possibly melanin, in the cuticle and a dark the plants on which they are reared (Grayson & Edmunds,
ommochrome in the epidermis, together with yellow and 1989), and the pupae of some butterflies that are not con-
orange pigments in the epidermis. The darkening of the cealed in a cocoon or in the soil, may be green, or dark or
stick insect, Carausius, which occurs on a dark background pale brown according to their surroundings.
is also due to the accumulation of two ommochromes, xan- An extreme example of homochromy occurs in African
thommatin and ommin (Bückmann, 1977). In this insect, grasshoppers after bush fires. Many species become black
changes occur at any time during the course of a stadium, within a few days, the change occurring in adults as well as
but in most other examples the change is first seen at a larvae, but only in bright sunlight. In diffuse light the
molt. Ommochrome deposition begins after about five change is much less marked.
days on the new background, and the changes in other All these changes depend on vision, although the
insects generally require a similar period of exposure. details may vary from species to species. In Carausius,
Caterpillars, too, may exhibit some degree of darkening results from weak stimulation, or the absence of
homochromy. Larvae of the popular hawk moth, Laothoe stimulation of the lower parts of the compound eye such as
populi, may be almost white or yellow-green depending on would occur when the insect is on a dark surface. In
SIGNIFICANCE OF COLOR 671
Gastrimargus, darkening occurs if a high incident light In some insects there are marked differences in color
intensity is associated with a low reflectance background, between successive generations correlated with seasonal
and changes in the yellow and orange pigments are depen- changes in the environment. Such seasonal polyphenism
dent on the wavelength of light. Homochromy in caterpil- and its physiological regulation is discussed in section
lars and lepidopteran pupae is also determined by the 15.5. Extreme cases of color polymorphism occur in some
wavelength of light and the contrasts in intensity reaching butterflies in relation to mimicry (see below).
the different stemmata.
The visual information affects the activity of neuro-
25.6 SIGNIFICANCE OF COLOR
scretory cells in the central nervous system. Homochromy
in pupae of the peacock butterfly, Inachis io, is produced by Insect pigments are often the end products of metabolic
changes in the relative amounts of melanin and lutein (a processes and may have evolved originally as forms of
carotenoid) in the cuticle. The accumulation of both pig- storage excretion. Pterins, for example, may be derived
ments is controlled by a single neuropeptide which is from purines, such as uric acid. Similarly melanin produc-
widely distributed in the central nervous system before tion might be a method of disposing of toxic phenols
being released into the hemolymph. A low hormone titer ingested or arising from metabolism and it may be
immediately before pupation stimulates melanization, a significant that melanin in the cuticle is often produced
higher titer results in increased incorporation of lutein above metabolically active tissue such as muscle.
into the pupal cuticle (Starnecker, 1997). Tryptophan in high concentrations reduces the rate of
development of Drosophila and Oryzaephilus and it is note-
25.5.2.3 Other factors affecting color worthy that ommochrome production follows the appear-
Temperature is important in pigment development and ance of unusually high levels of tryptophan in the tissues
there is a general tendency for insects reared at very high (Linzen, 1974). However, it is clear that storage excretion is
temperatures to be pale, and those developing at low tem- not the sole, or even primary function of pigments in most
peratures to be dark. Humidity affects the color of many insects. For example, most insects excrete most of the end
Orthoptera. Green forms are more likely to occur under product of the biologically active hydrogenated pterins and
humid conditions, and brown forms under dry conditions. do not store them. Pieris, on the other hand, synthesizes
Crowding influences color in some insects, the most much larger amounts than would result from normal
extreme examples being locusts. Locust larvae reared in metabolism and accumulates them in the wings, where they
isolation are green or fawn, while rearing in crowds pro- contribute to the color (Ziegler and Harmsen, 1969).
duces yellow and black individuals. The colors and pat- In most cases, the colors of present-day insects are
terns change as the degree of crowding alters (Stower, ecologically important. Color is most frequently involved
1959). The larvae of some Lepidoptera, such as Plusia and as a defence against vertebrate predators and it may also be
the armyworms, undergo comparable changes, some important in intraspecific recognition. It also has impor-
occurring in the course of a stadium, but the most marked tant consequences for body temperature, and color
alterations occur only at molting (Long, 1953). In caterpil- changes may contribute to thermoregulation (see above).
lars, these changes are known to be regulated by a neuro-
peptide. 25.6.1 Predator avoidance
In many species, color and color patterns have evolved as
25.5.3 Color polymorphism part of a strategy to avoid predation. The color patterns
Insects of many orders exhibit a green/brown poly- may function in a variety of ways in different insects: for
morphism, tending to be green at the wetter times of year concealment (crypsis), to deflect attack from the most
and brown when the vegetation is dry. The two forms are vulnerable parts of the body, to startle a predator, or to
genetically determined, but homochromy that develops advertise distastefulness.
when the insect moves to a new background may be super- Review: Edmunds, 1974
imposed on this. In green morphs the production of
ommochromes in the epidermis is largely or completely Crypsis Color often helps to conceal insects from preda-
inhibited; if it occurred, the green would be obscured. tors. Many insects are known to select backgrounds on
672 VISUAL SIGNALS: COLOR AND LIGHT PRODUCTION
which they are least conspicuous. Often, homochromy is Some Lepidoptera have a pattern of scales on the hind
associated with some appropriate body form and behav- wing forming an eyespot which is displayed when the
iour as in stick insects and many mantids and grasshoppers insect is threatened. One of the best known examples is the
which may be leaf-like or twig-shaped according to the peacock butterfly, Inachis io. It has one eyespot on the
backgrounds on which they normally rest. Protection may upper surface of each wing. These eyespots are primarily
also be afforded by obliterative shading. Objects are made black, yellow and blue, surrounded by dark red. The
conspicuous by the different light intensities which they butterfly rests with its wings held up over its back, the
reflect as a result of their form. A solid object usually looks upper surfaces of the forewings juxtaposed so that the eye-
lighter on the upper side and darker beneath because of the spots are concealed. If the insect is disturbed by visual or
effect of shadows, but by appropriate coloring this effect tactile stimuli it lowers the wings so that the eyespots on the
can be eliminated. If an object is shaded in such a way that forewings are displayed and then protracts the forewings to
when viewed in normal lighting conditions all parts of the expose the hindwing eyespots. At the same time the insect
body reflect the same amount of light, it loses its solid makes a hissing sound with a tymbal on the forewing
appearance. Such countershading is well-known in cater- (section 26.1.3.2). The forewings are then retracted and
pillars where the surface towards the light is most heavily partly raised and the sequence of movements repeated,
pigmented and the side normally in shadow has least sometimes for several minutes. While displaying, the body
pigment. To be successful in concealing the insect, this is tilted so that the wings are fully exposed to the source of
type of pigmentation must be combined with appropriate stimulation and at the same time the insect turns so as to
behavior patterns; if the larva were to rest with the heavily put the stimulus behind it. This eyespot display causes
pigmented side away from the light it would become more, flight behavior in at least some birds. Some mantids also
not less, conspicuous. Color may also afford protection if have a large eyespot on the hind wing.
the arrangement of colors breaks up the body form. Such
disruptive coloration is most efficient when some of the Deflection marks Small eyespots, often present on the
color components match the background and others con- underside of the hindwings of butterflies, appear to deflect
trast strongly with it. Disruptive coloration occurs in some the attention of birds away from the head of the insect.
moths which rest on tree trunks. There is no sharp distinction between eyespots used for
Review: Edmunds, 1990 deimatic behavior and those concerned with deflection. In
general, deflecting spots are probably smaller than those
Deimatic behavior Some insect species have colored used in intimidation, but it is possible that some may serve
wings, or other parts of the body, which are normally con- either function depending on the nature and experience of
cealed, but are suddenly displayed when a potential preda- the predator.
tor approaches. This behavior, sometimes associated with Some lycaenid butterflies have tails on the hind wings
the production of a sound, has been shown, in a few cases, and a color pattern that, at least to humans, has the illusion
to startle the predator. It is known as deimatic behavior. of the insect’s head. It is probable that this serves as a
In many insects exhibiting this behavior, the hindwing deflection device to some bird predators.
is deep red or black. It is normally concealed beneath the
forewing, but is revealed by a sudden partial opening of the Aposematic coloration Many insects are distasteful by
wings. This occurs in a number of stick insects and virtue of chemicals they produce themselves, or that are
mantids, and in moths that normally rest on vegetation. sequestered from their food; other insects sting (section
Moths in the family Arctiidae have bright red or yellow 27.2.7). Such insects are commonly brightly colored, and are
abdomens, often with black markings. When disturbed, usually red or yellow combined with black. Such coloration
the abdomen is displayed by opening the wings. The is a signal to predators that the potential prey is distasteful
deimatic display of some mantids involves the front legs and should be avoided. It is called aposematic coloration. For
which have conspicuous marks on the inside. Galepsus, for such coloration to be effective, the predator must exhibit an
example, displays the insides of the fore femora and coxae innate or a learned avoidance response. Aposematic species
which are orange, at the same time exposing a dark mark in occur in many orders of insects (Table 25.2).
the ventral surface of the prothorax. Reviews: Guilford, 1990; Rothschild, 1972
SIGNIFICANCE OF COLOR 673
Orthoptera
Zonocerus variegatus Adult B/Y and R markings Various chemicals
Romalea guttata Adult B/R hind wings Various chemicals
Hemiptera
Aphis nerii All Bright Y Cardiac glycosides
Oncopeltus fasciatus Adult Y/B spots Cardiac glycosides
Coleoptera
Coccinella septemfasciata Adult R/B spots Alkaloids
Tetraopes oregonensis Adult R Cardiac glycosides
Hymenoptera
Vespula vulgaris Adult Y/B stripes Sting
Lepidoptera
Tyria jacobaeae Larva B/Y stripes Pyrrolizidine alkaloids
Tyria jacobaeae Adult B/R marks Pyrrolizidine alkaloids
Battus philenor Larva R/B spots Aristolochic acids
Danaus plexippus Larva W/B and Y stripes Cardiac glycosides
Zygaena filipendula Adult B/R spots Cyanogenic glycosides
Note:
B, black; Y, yellow; R, red; W, white.
Mimicry Predators learn to avoid distasteful insects bug, Phonoctonus, lives with Dysdercus and preys on them.
with distinctive colors, but theoretically a predator must It, too is unpalatable to predators, and is a color mimic of
learn to avoid each individual species separately. If, Dysdercus so that avoidance of one leads to avoidance of
however, the color patterns of some species are similar to both species.
each other, learning to avoid one species because it is dis- In Batesian mimicry, only one of a pair of species is
tasteful also produces an avoidance of the other. distasteful, the other is not. They are called the ‘model’
Resemblance of one species to another is called mimicry. and ‘mimic’, respectively. Here, the palatable species gains
Mimicry takes two forms, Mullerian and Batesian. some advantage from a resemblance to a distasteful
Species exhibiting Mullerian mimicry are all distasteful. species. In this type of mimicry it is essential that the
Here, the advantage to the insects is that predation on any mimic is uncommon relative to the model. If this were not
one species is reduced. For example, many social wasp the case a predator might learn to associate a particular
species, such as Vespa and Vespula which all have a sting, pattern with palatability rather than distastefulness. This
have the same basic black and yellow pattern; if a predator limits the numbers or distribution of a mimetic form, but
learns to avoid one species, it is likely to avoid others with a the limit may be circumvented by the mimic becoming
similar appearance. Mullerian mimicry is also common polymorphic with each of its morphs resembling a differ-
amongst Lepidoptera, with the genus Heliconius having ent distasteful species. The best-known example of such
been especially well studied. Sometimes the mimics have polymorphism is that of the female Papilio dardanus
different life-styles. Cotton stainer bugs of the genus (Lepidoptera), which has a large number of mimetic
Dysdercus usually have similar red and black coloration and forms mimicking a series of quite different-looking
all the species are distasteful. The predaceous reduviid butterflies.
674 VISUAL SIGNALS: COLOR AND LIGHT PRODUCTION
Because the unpalatability of an individual may be 1957). Males of Colias eurytheme are attracted by the
affected by the nature of the food that it eats, mimicry may yellow underside of the female hindwing which is exposed
vary temporally and spatially. For example, the viceroy and when the female is at rest. In this species, the male reflects
queen butterflies of north America are both distasteful and ultraviolet from the upper side of its wings. This signal is
normally exhibit Mullerian mimicry (Ritland, 1991). used by the female in interspecific mate recognition, and it
However, sometimes larvae of the queen feed on plants also inhibits attraction by other males, reducing the likeli-
that are so low in the cardenolides sequestered by the hood of further male intervention when a male is copulat-
insect that the resulting adults are not distasteful. It may be ing (Silberglied & Taylor, 1978). It may be generally true
supposed that the palatable queen butterflies now depend that the colors of males are more important in male-male
for protection on their resemblance to other members of interactions than for recognition by females.
the species that have sequestered cardenolides, and on Review: Silberglied, 1984 – butterflies
unpalatable viceroy butterflies (Ritland, 1994).
Mimicry is common in Hemiptera, Hymenoptera,
25.7 LIGHT PRODUCTION
Diptera and Coleoptera as well as Lepidoptera. The model
and mimic are often in different orders. A number of insects appear to luminesce, but in many
Review: Turner, 1984 – butterflies cases this luminescence is due to bacteria. Self-lumines-
cence, not involving bacteria, is only known to occur in a
25.6.2 Intraspecific recognition few Collembola, such as Onychiurus armatus, in the
Color is important in intraspecific recognition in diurnally homopteran Fulgora lanternaria, in a few larval Diptera
active insects, and its role is most fully understood in dam- belonging to the families Platyuridae and Bolitophilidae,
selflies and dragonflies (Odonata), and in butterflies. In and in a relatively large number of Coleoptera, primarily in
both groups it has two principal functions in male behav- the families Lampyridae (fireflies), Elateridae and
ior: the recognition of females, and the recognition of Phengodidae (railroad worms). In these families lumines-
conspecific males. cence may occur in both sexes or be restricted to the
In some dragonflies, male color is important in defend- female; it also occurs in some larval forms.
ing a territory against other males. For example, the dorsal The light-producing organs occur in various parts of
side of the abdomen of male Plathemis lydia is blue. If a the body. Onychiurus emits a general glow from the whole
second male enters a territory, the resident male faces the body, but in most beetles the light organs are relatively
intruder and displays the color by raising the abdomen compact, and are often on the ventral surface of the
towards the vertical. This has an inhibiting effect on the abdomen. In male Photuris (Coleoptera), there is a pair of
intruding male. In the presence of a female, the abdomen is light organs in the ventral region of each of the sixth and
depressed so that the blue is not visible as the male seventh abdominal segments. In the female the organs are
approaches her. The females of many species change color smaller and often only occur in one segment. The larvae
as they become sexually mature and this is associated with have a pair of small light organs in segment eight, but these
a change in male behavior towards them. Amongst the disappear at metamorphosis when the adult structures
damselflies, the females of some species are dimorphic form. Larvae and females of railroad worms
with one of the morphs resembling the male, and there are (Phengodidae) have 11 pairs of dorso-lateral light organs
distinct differences in the behavior of males towards these on the thorax and abdomen and another on the head. In
two morphs (Robertson, 1985). Fulgora the light organ is in the head.
In butterflies, the general color of a female may be more The light organs are generally derived from the fat
important than the details of pattern in attracting males, body, but in Arachnocampa (Diptera) they are formed from
although size and movement are also important. For the enlarged distal ends of the Malpighian tubules.
example, males of the African butterfly, Hypolimnas mis-
ippus, are attracted by the female’s red-brown wing color; 25.7.1 Structure of light-producing organs in
the black and white markings sometimes present on the Coleoptera
forewings are unimportant, although white on the hind- Each light organ of an adult firefly consists of a number
wing may have an inhibitory effect (Smith, 1984; Stride, of large cells, the photocytes, which lie just beneath the
LIGHT PRODUCTION 675
dorsal layer
cells
trachea
granules
nerve
lumen of 'waste'
cylinder granules
photocyte
granules
end cell
tracheolar photocyte
cell
mitochondria
tracheole
epidermis
transparent
cuticle
Fig. 25.16. Diagrammatic section through part of the light organ on the ventral side of an adult Photuris. The tracheoles pass
between the photocytes, but do not penetrate into the cells (based on Smith, 1963).
epidermis and are backed by several layers of cells called plasma membranes of the end cell and the tracheolar cell
the dorsal layer cells (Fig. 25.16). The cuticle overlying the within which the tracheoles arise. In adult Pteroptyx
light organ is transparent. The photocytes form a series of (Coleoptera) and some other genera, nerve endings occur
cylinders at right angles to the cuticle with tracheae and on the photocytes as well as on the tracheal end cells.
nerves running through the core of each cylinder. Each The photocytes are packed with photocyte granules,
trachea gives off branches at right angles and as these enter each containing a cavity connecting with the outside cyto-
the region of the photocytes they break up into tracheoles, plasm via a neck. It is presumed that the reactants involved
which run between the photocytes parallel with the cuticle. in light production are housed in these granules. Smaller
The tracheoles are spaced 10 to 15 m apart and as the granules also occur dorsally and ventrally. Mitochondria
photocytes are only about 10 m thick the diffusion path are sparsely distributed except where the cell adjoins the
for oxygen is short. The origin of the tracheoles is enclosed end cells and tracheoles. The dorsal layer cells also contain
within a large tracheal end cell, the inner membrane of granules, generally regarded as urate granules, and it has
which is complexly folded where it bounds the tracheolar been supposed that the cells form a reflecting layer. There
cell (section 17.1.2). In some species, the end cells are only is, however, no direct evidence for this and it has also been
poorly developed. The neurons entering the photocyte suggested that the oxyluciferin irreversibly produced in
cylinder end as spatulate terminal processes between the light production (see below) is stored in them.
676 VISUAL SIGNALS: COLOR AND LIGHT PRODUCTION
male
Photuris versicolor
female
male
Photinus pyralis
female
0 5 10
time (seconds)
again. As the individuals produce flashes at regular inter- Females of Pteroptyx are attracted by the flashes of the
vals, this resetting rapidly results in synchronous flashing male group.
by all the insects. After mating, the females of some Photuris species
change their behavior so their patterning of flashing comes
25.7.4 Significance of light production to resemble that of females of other species (Vencl, Blasko
In most luminous insects light production has sexual & Carlson, 1994). In this way they lure males of those
significance. Light signals are used in two basic ways in species on which they then feed. The luminescence of
Lampyridae (Lloyd, 1971). In some species, such as Arachnocampa (Diptera) larvae also serves as a lure, attract-
Lampyris, the female is sedentary and attracts the male ing small insects into networks of glutinous silk threads on
to herself; in other species, such as Photuris and which they become trapped. The larvae then eat them.
Photinus, one sex, usually the male, flies around flashing In railroad worms, the lateral light-producing organs
in a specific manner. Flash duration and the interval may be suddenly illuminated if the insect is attacked, and
between flashes is often characteristic for the species they possibly have a defensive function. It is suggested that
(Fig. 25.18) and flashing is associated with distinct flight the red head light provides these insects with illumination,
patterns. For instance, male Photinus pyralis produce a presumably when they are searching for the millipedes on
flash lasting about 500 ms at six-second intervals. which they prey. The relatively long wavelengths emitted
During the flash the male climbs steeply and then by this organ may not be visible to most other insect preda-
hovers for about two seconds. If a female flashes 1.5 to tors, but the eyes of the railroad worms probably can detect
2.5 s after the male flash, he flies towards her and flashes them (Viviani & Bechara, 1997).
again three seconds later. He does not respond to flashes The sensitivity of the dark adapted compound eyes of
occurring after different time intervals. Repeated fireflies varies diurnally, as it does in at least some other
flashing sequences bring the male to the female. Precise insects. It increases rapidly by about four orders of magni-
timing requires a very well-defined time marker and tude at a time approximately corresponding with the time
flashes begin or end (sometimes both) sharply; these at which the insects normally flash (Lall, 1993).
transients probably provide the temporal signals. Review: Case, 1984
678 VISUAL SIGNALS: COLOR AND LIGHT PRODUCTION
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26 Mechanical communication: producing sound
and substrate vibrations
Many insects communicate using vibrational signals. environment (see below). If the sounds from the two sides
These may be air- or water-borne sounds, which are some- of the vibrating membrane are brought into phase with
times audible to humans, or they may be transmitted each other, constructive interference occurs, increasing
through the substrate on which the insect is resting. the intensity of the sound produced. This is achieved by
Sometimes the vibrations are purely adventitious, result- the cricket, Anurogryllus (see below).
ing from the insect’s normal activities, such as the sounds Reviews: Bailey, 1991; Ewing, 1989
produced by wing vibration in flight or by the mandibles of
an insect chewing, but they often have some special
significance for the insect and, in most cases, are produced 26.1 MECHANISMS PRODUCING VIBRATIONS
independently of other activities.
Vibrations may be produced in water and solids with 26.1.1 Percussion
little or no anatomical specialization. By contrast, insects Percussion refers to vibrations produced by the impact of
using airborne vibrations to communicate use structures part of the body against the substrate or by bringing two
and behaviors that enhance sound radiation. The structure parts of the body sharply into contact with each other.
transmitting vibrations to the air is known as the sound Many insects signal by striking the substrate with
radiator; it is often a part of the wing which is suspended some part of the body, usually without any related struc-
from the surrounding cuticle in a way that facilitates its tural modifications. Some termites and beetles use their
free vibration. heads. Soldiers of Zootermopsis, for example, make vertical
A sound radiator functions most efficiently in pro- oscillating movements using the middle legs as a fulcrum
ducing sounds with wavelengths similar to or less than its so that the head rocks up and down banging the tips of the
own dimensions. Consequently, because of their small
size, insects are constrained towards producing sounds
with short wavelengths (and high frequencies). However,
high frequency sounds attenuate more rapidly than lower
frequency, longer wavelength sounds so they are less good
for distance communication. In practice, airborne sounds
produced by different insects cover a very wide range of
frequencies and are often ultrasonic to humans (Fig. 26.1).
Sound is produced on both sides of a vibrating mem-
brane. If the membrane is small relative to the wavelength
of the sound produced, sound waves from the two sides
tend to interfere destructively because they are in anti-
phase. Such interference can be reduced or eliminated by a
baffle separating the air on the two sides of the membrane.
In many insects using part of the wing to produce sound,
the non-vibrating parts of the wing surrounding the Fig. 26.1. Range of airborne sounds produced by some insect
vibrating membrane may be used as a baffle. Some species groups, birds and humans. Within a group, not all species
extend the size of the baffle by employing structures in the produce the full range of frequencies.
[680]
MECHANISMS PRODUCING VIBRATIONS 681
substrate-borne vibrations are generally assumed to be sound radiation. Species of oecanthine crickets use leaves
unimportant. as baffles. They may simply choose a singing position
This method of producing vibrations is employed by between two leaves which then function as baffles, but
insects in many different orders, but is particularly associ- Oecanthus burmeisteri cuts a small hole in a leaf and, when
ated with Orthoptera, Heteroptera and Coleoptera. In one singing, sits with its head projecting through the hole and
insect or another almost every part of the body has become its tegmina tightly pressed against the leaf surface. It emits
modified to produce vibrations in this way. a sound with a frequency of about 2 kHz and a wavelength
of 170 mm. The sound-producing membrane on the wings
26.1.2.1 Stridulation in Orthoptera is only about 3 mm in diameter, but it uses leaves ranging in
The Orthoptera employ two main methods of stridulation: size from 70 ⫻ 80 mm to 170 ⫻ 300 mm and even the
tegminal stridulation in crickets (Grylloidea) and bush smallest of these is an efficient baffle (Prozesky-Schulze et
crickets (Tettigonioidea) and femoro-tegminal stridula- al., 1975).
tion in grasshoppers (Acridoidea). Anurogryllus produces complementary interference of
its song by standing in a saucer-shaped depression and
Crickets In male Grylloidea, each tegmen has a file on singing with the tegmina horizontal at a height equal to
the underside of the second cubital vein near its base, while one quarter of the wavelength of its principal frequency.
the ridge forming the scraper is on the edge of the opposite The sound waves from the underside of the wings are
tegmen (Fig. 26.3a,b). Mole crickets are able to use the reflected upwards from the saucer. These reflected waves
scraper on either wing by varying the relative positions of are in antiphase with the waves coming down and cancel
the wings, but in field crickets the right tegmen always them out, but they are in phase with the sounds produced
overlaps the left so that only the right field and left scraper on the upper side of the wing and so complement them.
are functional. In producing the sound, the tegmina are The mole cricket, Gryllotalpa vineae, amplifies its song
raised at an angle of 15–40º to the body and then opened by singing in a burrow shaped like an exponential horn
and closed so that the scraper rasps on the file. Sound is with two openings (Fig. 26.4). The dimensions of the horn
produced by both tegmina, each wing closure producing a are such that when the forewings are raised in the singing
single syllable of sound. position they form a diaphragm across it. The sound pro-
The principal sound radiator on the tegmen is an area duced has a fundamental frequency of 3–5 kHz, and is
of thick sclerotized wing membrane with no cross veins, amplified so that muscular energy is converted to acoustic
although sometimes with oblique veins. It is called the power with very great efficiency. As a result, the sound
harp and is enclosed by the first and second cubital veins carries over great distances, up to 600 m, and because of
(Fig. 26.3a). It is separated from the rigid subcostal, radial the tuning of the burrow the song is purer than when the
and medial veins, by a band of flexible cuticle so that it is insect is removed from the burrow. The sound is beamed
free to vibrate as a plate. In Gryllus, a more distal area of in an arc by the arrangement of the openings of the burrow.
thin cuticle, called the mirror, appears not to be specifically Female gryllids do not usually possess stridulatory
involved in sound production, although a comparable area apparatus, but male larvae of the later instars have the
in Tettigoniidae is very important (see below). apparatus and may stridulate.
The resonant frequency of the harp is approximately Review: Bennet-Clark, 1989
the same as the tooth impact frequency, and this contrib-
utes to the pure tones of most cricket songs (Fig. 26.3c) Bush crickets The stridulatory apparatus of
although the impact frequency may vary slightly during a Tettigonioidea is similar to that of gryllids, but the left
single wingstroke and from stroke to stroke. However, the tegmen overlaps the right and, in most fully winged forms,
airspace between the body and the raised tegmina also only the left file and the right scraper are present. In some
forms a resonator which both filters and amplifies the species, however, in which the hindwings are absent and
sound produced. The insect may thus be able to control the tegmina are short and rounded (Fig. 26.5), being
the frequency of its sound output by adjusting the volume retained only for the production of sound, a file and
of this space (Stephen & Hartley, 1995). scraper are present on each tegmen, although only the left
Some gryllids use environmental features to improve file is functional. The file of Platycleis has an average of 77
MECHANISMS PRODUCING VIBRATIONS 683
b) sound-producing apparatus
wing
movements
a) left tegmen right right file
scraper left
articulation with
thorax scraper
left file
right
left resonant tegmen
tegmen airspace
file (Cu 2 )
abdomen
scraper
mirror tooth
impact
sound intensity
flexible resonant
area frequency
of harp second
harmonic
0 5 10
frequency (kHz)
Fig. 26.3. Stridulation in crickets. (a) Left tegmen of Gryllus campestris seen from above. The file is on the underside of
Cu2 and so would not be seen in this view (after Bennet-Clark, 1989). (b) Diagrammatic cross section through an anterior
abdominal segment of a stridulating cricket. The sizes of the files and scrapers are exaggerated. The size of the airspace can
be varied so that it resonates at the frequency of the harp (not shown in this diagram). (c) Frequency spectrum of the sound
produced by Gryllus bimaculatus (after Stephen & Hartley, 1995).
teeth, and similar numbers of teeth are present in other next tooth impact occurs. The sound produced extends
species. Close to the plectrum on the right tegmen is an over a much wider range of frequencies than that of crick-
area of thin, clear cuticle known as the mirror supported ets (Fig. 26.5b) perhaps due to vibrations produced by
by a frame of thickened veins. As the scraper passes over different parts of the wing. The range often extends well
each tooth of the file, the frame is first distorted and then into the human ultrasonic range and may be entirely inaud-
returns to its original form, vibrating at its natural fre- ible to humans. The songs of Conocephalus species, for
quency as it does so. example, begin at about 20 kHz and extend above 100 kHz.
In most tettigoniids the natural frequency of the mirror As in gryllids, sound is generally produced on wing
and its frame is higher than the tooth impact frequency and closure, but sometimes, as in some individuals of Platycleis
each impact produces a short burst of sound waves (an intermedia and in Ephippiger (Fig. 26.5), a syllable of sound
impulse, Fig. 26.5a) which is rapidly damped before the is also produced on wing opening.
684 MECHANICAL COMMUNICATION
b) frequency spectrum
sound intensity
0 25 50
frequency (kHz)
Amongst Homoptera, frictional methods of stridula- function as a scraper and is no longer used in locomotion
tion occur in the aphid, Toxoptera, and most Psyllidae. (Fig. 26.8).
Review: Lyal & King, 1996 – Curculionidae
Coleoptera Stridulation occurs in many beetles, espe-
cially amongst Carabidae, Scarabaeidae, Tenebrionidae Lepidoptera The larvae and pupae of some Lepidoptera
and Curculionidae, and in the aquatic Dytiscidae and are able to stridulate. The caterpillars of lycaenid and rio-
Hydrophilidae. Different species use different parts of the dinid butterflies which are dependent on ants for their
body to produce sounds, but most commonly the elytra are development stridulate using a file on an abdominal
involved. In Oxycheila, for instance, there is a striated ridge segment. In Arhoplala, for example, a file on segment six is
along the edge of the elytron which is rubbed by a ridged rubbed by segment five. Caterpillars of species not associ-
area on the hind femur. ated with ants are not known to stridulate (DeVries, 1990).
Larval Lucanidae, Passalidae and Geotrupidae also Three main types of stridulation occur in pupal
stridulate, rubbing a series of ridges on the coxa of the Lepidoptera (Hinton, 1948). In ten families, notably the
middle legs with a scraper on the trochanter of the hind Hesperiidae, Papilionidae, Lymantriidae and Saturniidae
leg. In larval passalids the hind leg is greatly reduced to there are coarse transverse ridges on the anterior edges of
686 MECHANICAL COMMUNICATION
muscle and communicates with the outside via the meta- produced by a single contraction of the muscle, depending
thoracic spiracle. The presence of the airsac leaves the on the arrangement of the ribs (Fig. 26.10b, c). When the
tymbal free to vibrate with a minimum of damping. muscle relaxes, the tymbal is returned to its original position
Projecting back from the thorax on the ventral surface is by the dorsal resilin pad. This outward movement of the
the operculum, which encloses a cavity containing the tymbal also produces sound. In some species sound pro-
tympanum (used in sound reception) and an area of thin, duced on the outward movement is of such low intensity
corrugated cuticle, the folded membrane, which separates that it probably does not contribute to the biological signal,
the airsacs from the cavity beneath the operculum. When but in other cases it does appear to form part of the song.
the abdomen is raised the membrane is stretched. Buckling of the tymbal causes it to vibrate at its reso-
Sound is produced when the tymbal muscle contracts, nant frequency and this vibration is transferred to the
causing the tymbal to buckle inwards. Depending on the airsacs backing the tymbal. If their resonant frequency is
arrangement of the vertical ribs on the tymbal and on the close to that of the tymbal, the sound is greatly amplified.
tension exerted by the tensor muscle, the buckling may In the bladder cicada, Cystosoma, the airsacs are fused and
occur in a single movement or in a series of movements as fill the whole abdomen except for a small space dorsally
the ribs give way. Each component of the buckling may containing the viscera. By varying the volume of the
produce a pulse of sound, so one or several pulses may be airsacs, other cicadas can bring them in and out of tune so
688 MECHANICAL COMMUNICATION
a)
a) stridulatory
thorax
petiole apparatus
head
hind leg
leg
bases gaster
c) b) posterior wall
middle file of petiole
leg
b) scraper
scrapers
file on
coxa
anterior wall
of gaster
intersegmental
membrane
that sound intensity is modulated. In some cicadas, such as the natural frequency of the tymbal. In Cystosoma this is
Cyclochila, sound radiates from the tympani which also 850 Hz, while in Platypleura it is about 4500 Hz. The
function as hearing organs; the tymbals themselves are sound may be a relatively pure tone with few harmonics,
unimportant, but in other species both tymbals and but in other species a broad range of frequencies is pro-
tympani, as well as other parts of the abdomen wall, act as duced.
radiators (Young & Bennet-Clark, 1995). Amongst other Homoptera, tymbal mechanisms are
Repeated oscillations of the tymbal muscle produce a present in the males of all the Auchenorrhyncha examined
sustained sound. In most species, including Psaltoda and in both sexes of many families. In these insects the
where they oscillate at 225 Hz, the tymbal muscles are tymbals are not backed by airsacs and so damping of the
driven neurogenically (section 10.3.2.2), but in vibrations of the tymbals is very high. Tymbals are also
Platypleura, with an oscillation frequency of 390 Hz, the present in some pentatomids, cydnids and reduviids
tymbal muscles are myogenic fibrillar muscles. In some where they are on the dorso-lateral surfaces of the fused
species, the muscles of the two sides contract in synchrony, first and second abdominal terga with an airsac beneath.
while in others they contract alternately thus doubling the In these insects, tymbals usually occur in both sexes,
pulse repetition frequency. Some species are known to although often only those of the male are functional. The
vary the degree of synchrony between the two sides. vibrations are transmitted to the substrate, presumably
The frequency of the sound produced is determined by through the legs.
MECHANISMS PRODUCING VIBRATIONS 689
26.1.3.2 Tymbals of Lepidoptera range of frequencies from 30–90 kHz, but the overall spec-
Some Arctiidae have a tymbal on each side of the meta- trum extends from 11 to 160 kHz.
thorax (Fig. 26.11). It is covered by scales posteriorly, but Tymbals are also present in some Pyralidae. In the wax
anteriorly has a band of parallel horizontal striations, moth, Galleria, the tegula at the base of the forewing is
comparable with the vertical ribs on the tymbals of cicadas. modified to form a tymbal. No muscles are directly associ-
These vary in number in different species from 15 to as ated with it, but it is actuated by twisting the wing base
many as 60. presumably by the direct flight muscles. In males of
Buckling of the tymbal is not produced by a muscle another pyralid, Symmoracma, sound is produced by a
directly attached to it, as it is in the cicadas, but by the tymbal on the underside of the terminal abdominal
coxo-basalar muscle attached above and below it. When segment (Heller & Krahe, 1994).
this muscle contracts, the tymbal buckles inwards, starting Some butterflies, of which Inachis io (the peacock
dorsally and proceeding down the striated band, each rib butterfly) is the best known example, produce sounds
being stressed to the point of buckling and then suddenly as they open their wings due the buckling of a small area of
giving way and producing a pulse of sound. When the the forewing between the costal and subcostal veins.
muscles relax, the tymbal springs out due to elasticity and a
further series of pulses is produced. In Melese, the sounds 26.1.4 Vibrations produced by the flight muscles
produced on the IN movement show a progressive fall in In addition to the stridulatory movements of some
frequency, those on the OUT movement a progressive rise Orthoptera that involve the flight muscles (see above),
(Fig. 26.11b). Most of the sound produced lies within a oscillation of the flight muscles produces thoracic and
690 MECHANICAL COMMUNICATION
a) tymbal
100 ms
anepisternum
80 IN OUT IN OUT IN
bodied insects usually produce a higher intensity of sound
60 than soft-bodied insects.
Many Drosophila species and some trypetid flies
40
produce sounds when they are not flying by vibrating the
10 ms partially opened wings. Male D. melanogaster produces
sound with one wing extended sideways at 90º to the
Fig. 26.11. Tymbal organ of an arctiid moth (Melese) (after Blest,
body; the sound frequency is only about 100 Hz (Fig.
Collett & Pye, 1963). (a) Diagram of the left side of the
26.12). Drosophila erecta, which sings with its wings only
metathorax showing the position of the tymbal relative to the
surrounding sclerites. (b) Modulation of the principal frequency partially open, at 20–40º from the body axis, produces a
component of the sound produced. Each cycle is the result of one high frequency sound, about 450 Hz. These sounds are of
in–out movement of the tymbal. very low intensity and they are perceived as particle
movements by the antennae of the female. They may be
wing vibrations which may be used in communication by a produced as a continuous tone, or as a series of sound
number of insect species. pulses.
Vibration of the wings in flight produces a sound with a Honeybees use their flight muscles to generate vibra-
fundamental frequency the same as the frequency of the tions important in social communication (Fig. 26.13). A
wingbeat. However, other components may be added to worker bee returning from foraging performs a waggle
this fundamental frequency as a result of the varied struc- dance during which airborne vibrations are produced by
ture of different parts of the wing and the vibration of the the wings which are held horizontally over her back. These
thorax, so the overall sound produced is complex consist- vibrations have a frequency of 250–300 Hz, close to the
ing primarily of harmonics of the wingbeat frequency. The wingbeat frequency, and are produced in 30-second
flight noise of a locust, Schistocerca, with a wingbeat pulses. They are detected as near field sounds (particle
MECHANISMS PRODUCING VIBRATIONS 691
0.5
0
1s
-0.5
100 ms
100 ms
5s
100 ms
100 ms
Fig. 26.13. Vibrations produced by wing muscles of worker and queen honeybees (Apis). (a) Particle displacement in the near
field produced by workers performing the waggle dance. The variation in amplitude of alternate pulses results from the side-
to-side movement of the gaster (after Michelsen et al., 1987). (b) Substrate vibration produced as a stop signal (‘begging’) by
a bee following a dancer (after Michelsen, Kirchner & Lindauer, 1986b). (c) Tooting. A substrate borne vibration produced
by a young queen. Detail of the vibrations below (after Michelsen et al., 1986b). (d) Quacking. A substrate borne vibration
produced by a young queen. Detail of the vibrations below (after Michelsen et al., 1986a).
displacement) by the antennae of following workers who, a sound with a range of frequencies up to about 14 kHz and
at the same time, may produce stop signals (previously a maximum at 7–8 kHz. Vibrations of the epipharynx
known as begging calls). These, too, are produced by produce a series of sound pulses (Fig. 26.14). Contraction
vibration of the flight muscles, but are transmitted of the pharynx with the epipharynx held erect expels the
through the insects’ legs to the comb of the hive which air producing a whistle. These sequences are repeated
transmits the vibrations. rapidly.
Young virgin queen bees produce piping sounds by The hissing cockroach, Gromphadorhina, makes
thoracic vibration. The thorax is pressed to the comb so sounds by expelling air through the enlarged fourth
that vibrations are transferred directly to the comb. abdominal spiracle. The trachea leading from the
Queens that have escaped from the cells produce a ‘toot’; spiracle tapers to a narrow connection with the
those still in the cells produce a ‘quack’ which is a rapid longitudinal tracheal trunk. Air is forced through this
train of short periods of vibration (Fig. 26.13). connection when the expiratory muscles contract and
all other spiracles are closed, producing a hissing
26.1.5 Air expulsion noise. The frequency spectrum of the sound has a
The death’s head hawk moth, Acherontia, sucks air in maximum at about 10 kHz but extends up to about
through the mouth by dilating the pharynx. This produces 40 kHz.
692 MECHANICAL COMMUNICATION
100 ms
(1974) (Fig. 26.15). The sound of a single file tooth striking a) impulse - one tooth impact
the scraper is called an impulse; the sound produced by a
single up or down movement of a leg or by opening or
closing a wing is called a syllable; and the sound produced
by one whole sequence of leg movements, as shown in Fig.
26.16, is a chirp. Chirps may also be organized into higher
order sequences. 0.5 ms
The grasshopper, Chorthippus mollis, provides an
b) syllable - one down or up movement of leg
example of the mechanisms involved in producing a dis- (opening or closing wing)
tinctive song pattern. At the start of stridulation it pro- tooth
impacts
duces a sharp, high amplitude syllable of sound by moving
one leg sharply downwards (Fig. 26.16). It then makes
oscillating up and down movements with the femur which
gradually increase and then decrease in amplitude. These
5 ms
oscillations are superimposed on a slow raising and lower-
ing of the general position of the femur. As a result, differ- c) chirp - one complete cycle of leg (wing)
ent sections of the file strike the scraper and produce movements
sound syllables that vary in intensity. Towards the end of down up down up down up
leg 2
movements
leg 1
movements
levator
muscles
leg 1 abductor
muscles muscle
depressor
muscles
sound
Fig. 26.16. Muscular activity during stridulation by a grasshopper (Chorthippus mollis). Top: the activity of the two hind legs
during a single chirp which consists of a sequence of up and down movements of each leg superimposed on a slower upward
and downward movement. The effect of the slow upward movement is to bring progressively more proximal teeth of the
femoral file into contact with the scraper. In this species, the two legs are slightly out of phase. Center: the pattern of activity
in muscles moving leg 1. Each horizontal line represents a separate muscle. Each muscle is innervated by fast and slow axons
whose activity in recruiting the muscle units is shown by rectangles. Note that the greatest number of muscles and muscle
units are activated by the fast axons during the middle of the chirp when the amplitude of leg movements is greatest (above)
and the amplitude of sound greatest (below). The muscles are activated shortly before leg movement is observed. Bottom:
sounds produced by the movements of leg 1. The vertical axis shows the amplitude of sound. Syllables of sound are produced
on both the up- and downstrokes, but sound intensity is greatest on the downstroke (after Elsner, 1975).
PATTERNS OF VIBRATIONAL SIGNALS 695
a) grasshoppers
Stenobothrus
lineatus
Omocestus
viridulus
Chorthippus
brunneus
Chorthippus
parallelus
Fig. 26.17. The effects of temperature on sound production. The
frequency of syllable production (wing movements) produced by 1s
the cricket, Oecanthus (after Walker, 1962). b) crickets
Nephotettix
Grasshoppers – femur/tegmen stridulation Elsner, 1983
nigropictus
Cicadas – tymbal, airborne sound Claridge, 1985
Nephotettix Planthoppers – tymbal, substrate vibration Claridge,
virescens
1s 1985
Stoneflies – percussion, substrate vibration Szczytko &
female Stewart, 1979
Nilaparvata
lugens Lacewings – abdominal vibration, via substrate Henry,
male
1980
1s
Drosophila – wing vibration, near field Ewing, 1989
Fig. 26.20. Vibration patterns produced by tymbal organs. All
the insects have a basically similar mechanism for producing 26.3.2 Unorganized vibrations
vibrations. (a) Airborne vibrations produced by different species Many insect species produce vibrations, which may be air-
of cicada (after Young, 1973). (b) Substrate vibrations produced
borne or substrate-borne, that are not organized in precise
by planthoppers and leafhoppers. Javasella (Delphacidae),
temporal patterns (Fig. 26.7c). In these cases, the vibra-
Nephotettix (Cicadellidae) and Nilaparvata (Delphacidae) (after
de Vrijer, 1982; Claridge, 1983; Claridge, den Hollander &
tions themselves, in context, are sufficient to convey
Morgan, 1985). information to conspecifics or other species. Such sounds
may be produced by any of the mechanisms described
above.
abdomen increases the space between the abdomen and the
operculum, altering the resonant frequency of the airsacs
26.4 NEURAL REGULATION OF SOUND
so that they can be roughly tuned to the tymbal to increase
PRODUCTION
the intensity of sound. Each species has a characteristic
pattern of activity of these different muscles. The patterns of muscular activity resulting in sound pro-
Organized patterns of vibrations are also produced by duction are generated by pattern generators in the central
some insects that communicate via the substrate. This nervous system. In crickets, where the sound is produced by
occurs in Plecoptera and Neuroptera, in many Homoptera, movements of the forewings, the pattern generator is in the
and in honeybees. These insects generate vibrations using mesothoracic ganglion; in grasshoppers, where stridulation
different mechanisms – abdominal oscillations in involves movements of the hind legs, the generator is in the
Plecoptera and Neuroptera, tymbals in Homoptera (Fig. metathorax. The pattern generators are presumed to be
26.20), and the flight muscles in Apis, but in most cases they networks of interneurons whose output regulates the activ-
are transmitted to the substrate via the legs. ity of the motor neurons controlling the muscles.
In these cases a principal variant is the frequency with However, each of the muscles is made up of several
which discrete pulses of oscillation occur, each pulse being units innervated by fast and slow axons. As a result, the
NEURAL REGULATION OF SOUND PRODUCTION 697
coordination of other 2
activities pattern
generator
7
motor neuron
3 4
THORACIC
GANGLION
3 4 muscles driving sound-
producing appendage
auditory input
resulting from insect's
own song
force exerted by a muscle can be varied, and this affects tooth-impact frequency when it cannot hear its own song.
sound production. When a grasshopper produces a chirp, By adjusting this frequency and altering its wing position
the number of muscle units involved in the oscillating it is able to tune its song (Stephen & Hartley, 1995). In the
movements of the femur, and their activation via fast cicada, Cystosoma, the frequency of oscillation of the
axons, first increases and then decreases (Fig. 26.16). tymbal, maintained by a central pattern generator in the
These changes, with slight changes in the timing, produce metathoracic ganglion, is modulated by feedback from a
the alterations in up and down movements during the chordotonal organ inserted on the rim of the tymbal.
chirp. Variation in the activity of other muscles, the coxal Singing is initiated by descending interneurons from
adductor and abductor muscles, produces changes in the brain, known as command neurons (Fig. 26.21). In a
sound intensity by pulling the coxa towards or away from male cricket, different command neurons initiate different
the body and varying the pressure of the femur against the songs. In addition, at least in grasshoppers, it is probable
tegmen. that output from the metathoracic pattern generator is fed
Although the basic movements are controlled by a forwards to the subesophageal ganglion and then redistrib-
pattern generator, they are modulated by sensory feedback uted to other parts of the body. This information may
from proprioceptors. In crickets, a hair plate and campani- provide positive feedback resulting in increased amplitude
form sensilla on the tegmina are essential for the produc- of leg movements and may also be involved in coordination
tion of normal song. In addition, at least in some species, of the left and right legs. It probably also permits coordina-
the sound of the insect’s own song is important. Gryllus tion of other activities with those directly involved in
bimaculatus, for example, is less well able to regulate its stridulation (Lins & Elsner, 1995).
698 MECHANICAL COMMUNICATION
Both external and internal factors are important in regu- species of Drosophila, D.pseudoobscura and D.persimilis.
lating song production. Males only sing when they are sexu- Some populations of the brown planthopper of rice,
ally mature and, in grasshoppers, there is a brief interruption Nilaparvata lugens, exhibit little interbreeding, even in the
of singing after copulation. Males of Gryllus campestris only laboratory, and it appears that differences in the patterns of
sing when they are carrying a spermatophore. After copula- substrate borne vibrations produced by the different
tion, when the spermatophore is transferred to the female, populations are primary isolating mechanisms (Claridge,
singing stops. Female grasshoppers only sing when they are den Hollander & Morgan, 1985).
in a sexually responsive state and, like other aspects of sexual These three examples demonstrate that airborne
maturation in these insects, it is possible that singing is regu- sounds, in both the far field (Chorthippus) and near field
lated by juvenile hormone. (Drosophila), and substrate-borne vibrations can contrib-
Review: Kutsch & Huber, 1989 – crickets ute to sexual isolation.
lepidopterous pupae, are presumed to be concerned with The sound frequencies produced by the tymbals of
defence against predators, inducing a startle response. some arctiid moths are within the range of the signals pro-
This type of sound production sometimes accompa- duced by echolocating bats. The moths respond to a bat’s
nies visual displays employed against predators (section signals with clicks of sound causing the bat to veer away.
25.6.1). In Arctiidae, sound production by the tymbal The mechanism by which the bat’s behavior is altered is
organs may be associated with a display of warning colors. not fully understood.
These are distasteful species and it is generally true that Although interspecific vibrational signals usually have
sounds are more readily elicited from the less distasteful a defensive role, those produced by some caterpillars are
species amongst them. Sounds associated with visual exceptional. The larvae of Riodinidae and Lycaenidae that
display are also produced by some mantids and grass- develop in association with ants use substrate vibrations to
hoppers. attract ants. Species not tended by ants do not stridulate
There is also the suggestion that sound mimicry (DeVries, 1990). Bumblebees use vibrations of the body
occurs. For example, not only do certain syrphids look like produced by oscillation of the flight muscles to displace
bees, they also sound like them, and the sounds produced pollen from the anthers of some flowers. This process,
by Nicrophorus when it is disturbed are similar to those of a known as buzz pollination, requires the bee to make bodily
torpid bumble bee, to which the beetle also bears a super- contact with the anthers either by gathering them to its
ficial visual resemblance. Whether these resemblances are body with the legs or by grasping an anther with the
due to selection or to chance similarities is not known. mandibles (King, 1993).
REFERENCES
Agee, H.R. (1971). Ultrasound produced Belton, P. (1986). Sounds of insects in Claridge, M.F. (1983). Acoustic signals
by wings of adults of Heliothis zea. flight. In Insect Flight: Dispersal and and species problems in the
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London: Chapman and Hall. communication in the death-watch courtship signals and hybridization
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Schilliger, E. (1988). Substrate vibra- London B, 158, 196–207. their acoustic characteristics in sibling
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DeVries, P.J. (1990). Enhancement of Heller, K.-G. (1996). Unusual abdomino- Lees, D.C. (1992). Foreleg stridulation in
symbioses between butterfly caterpil- alary, defensive stridulatory mechanism male Urania moths (Lepidoptera:
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Dumortier, B. (1963a). Morphology of Pseudophyllidae). Journal of Leston, D. (1957). The stridulatory mecha-
sound emission apparatus in Morphology, 227, 81–6. nisms in terrestrial species of
Arthropods. In Acoustic Behaviour of Heller, K.-G. & Krahe, R. (1994). Sound Heteroptera. Proceedings of the Zoological
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Dumortier, B. (1963b). The physical of Experimental Biology, 187, stridulatory interneurons in the sub-
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Verlag.
27 Chemical communication: pheromones and
chemicals with interspecific significance
Hormones are concerned with regulation within the are called releaser pheromones; those that affect metabo-
organism. Other chemical substances are concerned with lism are known as primer pheromones.
communication between organisms, both intra- and inter-
specifically. Chemicals with an intraspecific function are 27.1.1 Structure and distribution of pheromone
called pheromones; those with an interspecific function glands
are often called allelochemicals. Some chemicals can serve In most insects, pheromones are produced by glandular
both functions, even in one insect (Blum, 1996). Most epidermal cells concentrated in discrete areas beneath the
pheromones and allelochemicals are produced by ectoder- cuticle, but, in some species, gland cells are scattered
mal glands secreting to the outside of the body. The basic through the epidermis of different parts of the body. In
structure of these exocrine glands is similar irrespective of male desert locusts (Schistocerca gregaria), for example,
whether they produce pheromones or allelochemicals, but class 3 gland cells (section 16.1.1) are scattered over the
their positions on the body and the chemicals they produce head, thorax and abdomen. In an immature insect, they are
exhibit extraordinary diversity. Glands producing chem- small and restricted to the basal part of the epidermis, but
icals for interspecific communications usually have reser- as the insect matures they enlarge and extend distally
voirs while most pheromone glands do not. Pheromones towards the cuticle. The cytoplasm in a mature insect,
used for marking, however, are usually stored in a reser- viewed with the electron microscope, contains large
voir. Many chemicals used for defense are stored within numbers of electron-dense granules with numerous clear
the body and are not secreted. vesicles close to, and probably discharging into, a terminal
cavity. The contents of the cavity are discharged on the
surface of the cuticle via a ductule. Similar scattered glands
27.1 PHEROMONES
are present in some Heteroptera. In the higher Diptera, the
A pheromone is a secretion which, if passed to another cuticular hydrocarbons forming the sex pheromone are
individual of the same species, causes it to respond, produced by epidermal cells, primarily in the abdomen.
physiologically or behaviorally, in a particular manner. Where the secretory cells are aggregated to form a
Pheromones are thus concerned with signalling between gland, they are usually class 1 gland cells (section 16.1.1)
individuals of the same species and are therefore often without ducts to the exterior and abutting directly on to
important in sexual behavior and in regulating the behav- the cuticle. The glands are often concealed beneath a fold
ior and physiology of social and subsocial species. It is of cuticle, such as an intersegmental membrane between
probably true that pheromones are used in communication abdominal segments. They have no reservoir and the
by at least some species in all the insect orders. pheromone is released directly following its synthesis. In
Many pheromones are perceived as scents by olfactory other cases, the glands open into an epidermal invagina-
receptors and affect the recipient via the central nervous tion which may then serve as a reservoir in which the
system. In other cases, pheromones are ingested by the pheromone accumulates. This is the case with the marking
recipient. These may be perceived by the sense of taste, pheromone of social Hymenoptera where larger quantities
exerting their effects via the central nervous system, or the of pheromone are produced.
pheromone, once ingested, may be absorbed and influence In many female Lepidoptera, the glands producing the
biochemical reactions within the recipient. Pheromones male sex attractant pheromone lie beneath an interseg-
which affect behavior directly through the nervous system mental membrane of the posterior abdominal segments,
[704]
PHEROMONES 705
propharyngeal gland
enzymes
pygidial gland
alarm pheromone
metapleural gland
antibiotics
maxillary
gland Pavan's gland Dufour's gland
trail pheromone alarm pheromone
mandibular gland
alarm pheromone
gland
cells
reservoir
applicator
surface
gaps in cuticle
forming reservoir tergum 7
Fig. 27.2. Exocrine glands of worker ants. (a) Longitudinal section of a worker ant showing the principal glands with dark
shading. All the glands shown may not be found in one species. Examples of the functions of secretions from the glands are
shown in italics, but note that the secretion from a particular gland may serve different functions in different species (based on
Hölldobler & Wilson, 1990). (b) Pygidial gland of a worker ant, Pachycondyla (based on Hölldobler & Traniello, 1980). (c)
Poison gland and Dufour’s gland of a worker ant (Myrmica). The organization of the gland is simpler than that depicted in (a)
(based on Billen, 1986).
simple sac with thin glandular walls and a delicate muscu- pygidial gland with a similar structure, the ducts from the
lar sheath. cells opening into a reservoir between abdominal tergites
Worker honeybees have a gland, Nasonov’s gland, six and seven (Fig. 27.2b).
beneath abdominal tergite six which is exposed by Review: Percy-Cunningham & MacDonald, 1987 – sex
depressing the tip of the abdomen. It is made up of about pheromone glands
500 large class 3 gland cells each with a duct to the surface
of the cuticle (Fig. 27.3b). Oenocytes and fat body cells are 27.1.2 Chemical characteristics of pheromones
closely associated with the gland cells, but the gland is not There is great variety in the chemicals used as pheromones
innervated (Cassier & Lensky, 1994). Most ants have a depending on species, function and mode of action. The
PHEROMONES 707
tergum 6
mandibular
gland
tergum 7
Nasonov
opening of gland
gland ducts
cuticle
groove epidermis
mandible
gland
cell
depression
fat body
cell
oenocyte
Fig. 27.3. Two exocrine glands of worker honeybees: (a) mandibular gland and mandible (after Snodgrass, 1956);
(b) Nasonov gland, with part of the gland enlarged (below).
chemical nature of volatile pheromones is, to some extent, Most pheromones are mixtures of compounds, some-
constrained by the conflicting requirements of volatility times only two, but sometimes as many as ten. The compo-
and specificity. Small molecules are more volatile, but the nents may all be similar and, perhaps, derived through a
number of structural variations which they can form is single synthetic pathway (see Table 27.1; Fig. 27.7), but
limited. The appropriate degree of specificity can only be chemicals of more than one class may also be present. The
achieved with larger molecules which allow more variation. different components of a pheromone are sometimes
Hence the molecular size of many volatile pheromones known to act synergistically, and in other cases evoke
represents a balance between the two opposing require- different responses from the recipient (see Fig. 27.13).
ments of volatility and specificity. The degree to which
these features are required depends on the particular func- Aliphatic hydrocarbons Aliphatic hydrocarbons are used as
tions of the pheromone in question. Sex attractant pheromone components by many insects. The sex attractant
pheromones are, of necessity, both specific and volatile. pheromones of many female Lepidoptera are straight chain
Alarm pheromones, by contrast, should be highly volatile hydrocarbons, most commonly with chain lengths of 12, 14
in order to alert other nearby insects to a source of danger, and 16 carbon atoms (Fig. 27.4). Most moth pheromones are
but also to minimize the period of disruption. They do not acetates. Hydrocarbons of similar size are the sex
need, therefore, to be highly specific and consequently tend pheromones of some Coleoptera, but, in these insects, the
to be made up from small, highly volatile compounds. compounds are often methylated. Short-chain molecules also
Marking pheromones, such as oviposition deterrents and form the pheromones of scale insects (Coccidae,
trail pheromones, on the other hand might be expected to Homoptera), sawflies and the honeybee where the principal
be specific, but less volatile as their persistence is a requi- sex attractant is 9-oxodecanoic acid. In most bumblebees, the
site. In some cases, however, persistence is achieved main components of the marking pheromone are hydro-
through continual remarking. Contact pheromones are not carbons with chain lengths of 16, 18 or 19 carbon atoms. The
constrained by the need for volatility (see Fig. 27.4). scent scales of some male pierid butterflies contain alkanes
The chemical components of pheromones are, in with chain lengths of 10 to 13 carbon atoms. In
most cases, not unique and the same compound may be Tenebrionidae (Coleoptera) and Pentatomidae (Hemiptera)
used by a variety of species. Aliphatic hydrocarbons and short-chain aldehydes function as aggregation pheromones.
terpenoids are most commonly employed, but a variety of Shorter chain length hydrocarbons are often used as
other chemical classes are used by different insect species. alarm pheromones. Amongst the Heteroptera, hexenal
708 CHEMICAL COMMUNICATION
40 loids.
27.1.3 Specificity
Communication within a species requires specificity of the
20
signals. With pheromones, this specificity is achieved in
two ways: on the basis of molecular structure, and by
specific mixtures (blends) of compounds. This demands
0 not only that the sender should produce specific chemicals
1 6 11 16 21 26 31 36
in appropriate proportions, but also that the neural system
chain length (number of carbon atoms)
of the receiver is tuned to the appropriate blend.
lepidopteran sex pheromone Specificity has been studied most in the sex attractant
cyclorrhaphan Diptera
pheromones of Lepidoptera. Four characteristics of the
ant alarm pheromone
molecule are of particular importance: chain length, the
Fig. 27.4. Chain lengths of aliphatic hydrocarbons used as alarm nature of the functional groups, the number and position
pheromones by ants, long-range sex attractants by moths, and of double bonds, and the configuration of the bonds. For
contact pheromones by cyclorrhaphan Diptera. the families Noctuidae, Pyralidae and Tortricidae, the
major pheromone component has 10, 12, 14, 16 or 18
and octenal have been identified as components of alarm carbon atoms in a straight chain (Fig. 27.5). The func-
pheromones; in bees there are short chain (5–9 carbon tional group is usually a primary alcohol, an aldehyde, or
atoms) acetates, alcohols and ketones; and myrmicine ants acetate, and there may be one, two or three double bonds in
produce ketones with chain lengths of 6–9 carbon atoms. a variety of positions. This combination of characters pro-
Formic acid is a component of the alarm pheromone of vides an enormous range of different compounds, and
formicine ants; it is also used as a defensive chemical. neural receptors in the receiver may be highly specific (see
At the other extreme, the contact or short-range sex Fig. 24.6).
pheromones of some calypterate Diptera are alkanes or Specificity also results from the use of particular blends of
alkenes with odd-numbered chain lengths of more than 20 compounds. Closely related, sympatric species may produce
carbon atoms, and, in many species, more than 30. pheromones with the same suite of chemicals but differing in
the proportions of the components. Table 27.1 illustrates
Aromatic hydrocarbons Aromatic hydrocarbons have not some of these points in relation to the moth genus,
been widely reported as pheromones, but they do occur in Spodoptera. The chain lengths for the major components of
the male scent brushes of a number of noctuid moths. most species are the same, 14 carbon atoms, but the North
Phenyl ethanol, benzyl alcohol and benzaldehyde are American S.frugiperda is distinct as its primary component
examples. has only 12 carbon atoms. In all species, acetate is the func-
tional group on the major compounds and the principal
Terpenoids Mono- and sesquiterpenes are commonly differences lie in the number of double bonds, their positions,
used as components of alarm pheromones. This is true for and the proportions of the different compounds. Except for
aphids, termites and formicine ants. Some ants also use S.littoralis and S.litura, all the species are distinguishable
terpenes as trail pheromones, and they are the marking from these characteristics and, presumably, have the capacity
compounds used by a few bumblebees. Bark beetles use a to distinguish conspecific from heterospecific insects. The
variety of monoterpenoid compounds as attractants and geographic ranges of the species do not all overlap, so that
aggregation pheromones, and this is also true of the cotton some species never encounter others. For example, S.litura
boll weevil, Anthonomus. occurs in eastern Asia, while S.littoralis is west Asian and
African, and perhaps this geographical separation makes it
Nitrogen-containing cyclic compounds A number of ants possible for the two species to have such similar pheromones.
use heterocyclic nitrogen compounds as trail pheromones, Spodoptera descoinsi and S. latifascia, however, are sympatric
PHEROMONES 709
Chain length 12 14 14 14 14 14 14 14 14 14 14 16
Double bond Z9 — Z9 Z9 Z9 Z9 Z9 Z9 E9 Z11 E11 Z11
E11 E12 Z12 E12
Functional groupb ac ac ac ald ol ac ac ac ac ac ac ac
descoinsi 41 2 1 42 3 ⬍1 11
eridania 80 20
exempta 95 5
exigua 48 4 40 6 2
frugiperda 90 10
latifascia 78 8 1 7 1 ⬍1 8
littoralis ⫹ ⫹ 95 ⫹ ⫹ ⫹
litura 91 9
Notes:
a Numbers give percentage of each component. For most species they represent the amounts
b) functional groups
C C C C C C C
tetradecanol (14ol)
C C C C C C C OH
C C C C C C C
tetradecanal (14ald)
C C C C C C C H
O
carbon
c) double bonds atom 9
C C C C C C O CH 3
Z-9-tetradecenyl acetate
(Z 9-14ac) C C C C C C C C C
carbon carbon O
atom 11 atom 9
C C C C C C O CH 3
Z,E-9,11-tetradecadienyl acetate
(Z 9,E 11-14ac) C C C C C C C C C
O
710 CHEMICAL COMMUNICATION
C C C C C C
C C C C C C C
O O
OH
homonerol oxide
Z 6 - undecenol
Z 6 - tridecenol
nerol oxide
homonerol
nerol
Acanthaclisis occitanica + +
Euroleon nostras + +
Grocus bore + +
Myrmeleon formicarius + +
Synclysis baetica + +
and they will interbreed in captivity. They are clearly dis- hydrocarbon pheromones of many Lepidoptera and
tinguishable from the relative proportions of Z9-tetradecyl Diptera, for example, are synthesized from fatty acids in a
acetate and Z9,E14-tetradecyl acetate and presumably this series of steps. These involve chain shortening or elonga-
difference contributes to sexual isolation in the field. tion, desaturation and, finally, the modification of the
Sometimes the blend includes structurally different functional group by reduction, acetylation or, sometimes,
chemicals. For example, the male attractant pheromones of oxidation (Fig. 27.7).
antlions contain two compounds, which, in some species, are Honeybees produce mandibular gland pheromones
an aliphatic alcohol and a monoterpene. Specificity is con- from stearic acid. In workers this is hydroxylated at the
ferred by small differences in the structure of these molecules terminal (C18) position, while, in queens, C17 becomes
(Fig. 27.6). hydroxylated. The products become shortened to chains
of 10 carbon atoms and desaturated at the 2 position to
27.1.4 Origins of pheromone chemicals produce 10-hydroxydecenoic acid in the workers and 9-
Pheromones may be synthesized de novo in the glandular hydroxydecenoic acid in queens. Oxidation produces other
cells, or derived from precursors present in the food. Many related chemicals (Plettner et al., 1996).
pheromones with ring structures are known to be derived Ants synthesize the terpenoids that often contribute to
from such precursors, but there is also evidence, in some their alarm pheromones.
cases, that the insects can synthesize them. In other cases,
symbiotic microorganisms may contribute to synthesis. Pheromone precursors from food Some insects are known
to require specific chemicals from their food which are
Pheromone synthesis Most pheromones of most insects then modified to form pheromones.
are synthesized de novo from smaller molecules. The Many of the compounds in the pheromones of male
PHEROMONES 711
O
OXIDATION
C C C C C C C C
C C C C C C C C
C C C C C C C O CH 3 C C C C C C C C C C C C C C
C C C C C C C C C C C C C C C C C C C C C C C C
tetradecenyl acetate O O O
REDUCTION and
ACETYLATION DESATURATION CHAIN SHORTENING
C C C C C C C O CH 3 C C C C C C C C C C C C C
C C C C C C C C C C C C C C C C C C C C C C C
E 11 - tetradecenyl acetate O O O
C C C C C C C C C C C C O CH 3
C C C C C C C C C C C C C C C C C
O Z 9 - tetradecenyl acetate O
REDUCTION and
ACETYLATION
C C C C C C O CH 3
C C C C C C C C C
Z 9, E 11 - tetradecenyl acetate O
Fig. 27.7. Pheromone synthesis. Synthesis of different components of the sex attractant pheromone of Spodoptera littoralis
from a fatty acid. The processes occurring at each step are shown in capitals, and names of the final products are in bold type.
Open arrows show the stage which is probably regulated by the pheromone biosynthesis activating neuropeptide (based on
Fabriás, Marco & Camps, 1994).
Lepidoptera that have androconial brushes are derived from and ipsdienol from myrcene, and cis-verbenol from ␣-
chemicals in the larval food. These may be commonly occur- pinene, but Ips duplicatus synthesizes similar pheromones
ring compounds, such as benzaldehyde, benzyl alcohol and de novo (Ivarsson & Birgersson, 1995).
butyric acid used by a number of Noctuidae, but, in other In Reticulitermes an unsaturated alcohol, cis–3, cis–6,
cases, the pheromones are derived from compounds trans–8-dodecatrienol, which occurs in wood infected with
characteristic of the host on which the larvae feed. For the fungus Lenzites, is used as a trail pheromone.
example, some arctiid moths use pyrrolizidine alkaloids from
their host plants as pheromone precursors. The males of Synthesis by microorganisms Bacterial symbionts in the
many danaid butterflies also synthesize their pheromones hindgut of some bark beetles and the beetle, Costelytra,
from pyrrolizidine alkaloids (Fig. 27.8), but in these species are able to synthesize some of the compounds used by
the larvae do not feed on plants containing the alkaloids. their host insects as pheromones. It seems to be generally
Instead, they are acquired by the adult males, which lick alka- true, however, that the host insects are also capable of syn-
loid-containing plants. thesis and the relative importance of the symbionts is
Bark beetles and the boll weevil, Anthonomus grandis, unknown.
also produce pheromones from resins of their host plants Reviews: Prestwich & Blomquist, 1987; Schneider, 1987 –
(Fig. 27.8). Ips paraconfusus, for example, derives ipsenol Lepidoptera, alkaloids; Wood, 1982 – bark beetles
712 CHEMICAL COMMUNICATION
CH3 CH3
CH
O CH3
Danaus OH N
chrysippus
N danaidone
O OH
OH
H
Anthonomus
grandis
dimethyl- dimethyl-
geraniol cyclohexaneacetaldehyde cyclohexaneethanol
Ips
paraconfusus
HO
α-pinene H verbenol
Fig. 27.8. Pheromones derived from chemicals in plants. Top: pyrrolizidine alkaloids obtained from a plant by adult male
Danaus chrysippus. Center: geraniol, a monoterpene, in cotton is a source of pheromone components of the boll weevil,
Anthonomus grandis. Bottom: ␣-pinene, a monoterpene, in pine bark is a source of pheromone components in the bark beetle,
Ips paraconfusus.
27.1.5 Control of synthesis and release female H. zea produce increasing amounts of pheromone
Release of pheromones into the environment involves two each night for the first three nights after eclosion, but
separate processes: synthesis and dispersal. Where the mating almost completely inhibits further production.
pheromone gland is not associated with a reservoir, syn- The enzymes necessary for pheromone synthesis are
thesis often leads directly to dispersal, but, where a reser- produced late during development of the pharate adult,
voir is present, the pheromone may be stored, and and the development of competency to produce
synthesis and dispersal are temporally separated. pheromone is regulated by the falling titer of ecdysteroids.
The system is subsequently controlled by a peptide,
27.1.5.1 Pheromone synthesis pheromone biosynthesis activating neurohormone
In some female moths, such as Trichoplusia ni, pheromone (PBAN) which is produced by cells in the subesophageal
synthesis is continuous and the amount present in the ganglion. The method by which it affects the abdominal
gland at any time represents the balance between synthesis pheromone gland is unclear; it may be released into the
and release. Consequently, pheromone accumulates hemolymph via the corpora cardiaca, or, in those instances
during the daytime, when none is released, and then where the pheromone glands are innervated, may be trans-
decreases during darkness as a result of pheromone release mitted neuronally directly to the glands.
(Fig. 27.9a). In other species, such as Helicoverpa zea, syn- PBAN regulates the enzymes involved in pheromone
thesis only occurs at particular times of day (Fig. 27.9b), synthesis. In some species, such as Helicoverpa, it appears
which vary with the insect’s age and mated status. Virgin to govern the production of intermediates from fatty acids,
PHEROMONES 713
0 0
0 5 10 15 20 27.1.5.2 Pheromone dispersal
time (hours) Dispersal of pheromones into the environment involves
specific behavior and is often enhanced by cuticular struc-
calling
pheromone tures.
Where the gland cells are of class 3, with a duct extend-
Fig. 27.9. Temporal variation in calling behavior and amounts of ing to the surface of the cuticle, the pheromone can pass
pheromone in the glands of two nocturnal noctuid moths. freely on to the surface of the cuticle. Where, as in many
(a) The quantity of pheromone in the gland increases during the glands, the gland cells are class 1 and have no ducts, the
photophase, but declines during the scotophase when the females cuticle contains large numbers of wax canal filaments or, as
are calling. Pheromone synthesis is continuous (Trichoplusia ni)
in the glands producing the honeybee alarm pheromone, it
(data from Hunt & Haynes, 1990) . (b) Pheromone synthesis is
may be perforated by enlarged pore canals (Cassier, Tel-Zur
synchronous with calling behavior. None accumulates in the
& Lensky, 1994). In all these cases, the pheromone passes
gland during the photophase (Helicoverpa zea) (data from Raina,
Davis & Stadelbacher, 1991). through the cuticle very quickly after it is synthesized.
Dispersal of volatile pheromones from the surface of
but in others it acts at the stage of reduction and acetyla- the cuticle is believed to be facilitated by microtrichia.
tion shown in Fig. 27.7 (Fang, Teal & Tumlinson, 1995). These may be on the cuticle immediately above the gland,
The release of PBAN is regulated by environmental as in the abdominal glands of some female Lepidoptera, or
factors, especially daylength. Host-plant odors may also they may be on an adjacent part of the cuticle, as is the case
stimulate its release. with the alarm pheromone of the honeybee (Lensky,
Other factors may be involved in pheromone synthesis Cassier & Tel-Zur, 1995). The peak rate of release of the
and release. The amount of octopamine, which is known to sex attractant pheromone by female Trichoplusia ni into the
stimulate pheromone production, reaches a peak in the air is about 10 ng min⫺1, but it is considerably lower in
pheromone gland of Helicoverpa just before the start of the some other moths.
scotophase (Christensen et al., 1992). In Manduca, experi- Many male Lepidoptera have modified scales which are
mental neural stimulation of the gland also leads to the known or (more frequently) inferred to be involved in
714 CHEMICAL COMMUNICATION
Short-chain, unsaturated compounds in general have by the females of some species and the males of others
higher volatility than longer chain, saturated molecules. (Farine et al., 1994). Aliphatic hydrocarbons and terpenoids
This affects the rate of evaporation of different com- are commonly used as sex attractants (Table 27.2), the
pounds from the surface of a pheromone gland. The rate insects within a particular group tending to use similar com-
of emission also varies with temperature, but the effect of pounds although in the Lepidoptera and Coleoptera
temperature differs between compounds so that small different families may use different compounds.
changes in the ratios of the components of a blend occur These pheromones are only released when the insect is
(Liu & Haynes, 1994). ready to mate and at a time of day appropriate for the
Reviews: Birch, Poppy & Baker, 1990 – moth androconia; species. Virgin female Aphis fabae, for example, do not
Boppré, 1984 – butterfly androconia exhibit calling behavior for the first three or four days of
their adult life, but after seven days call regularly by raising
27.1.6 Functions of pheromones the abdomen and hind tibiae, (Thieme & Dixon, 1996).
27.1.6.1 Pheromones affecting behavior They call mainly in the morning, although there are
Releaser pheromones are commonly involved in various differences between subspecies. Most moths call only at
aspects of sexual behavior, but also occur in relation to night (Fig. 27.9). At least in some species, calling behavior
other aspects of behavior necessitating communication occurs independently of the amount of pheromone in the
between insects of the same species. gland indicating that regulation of calling and pheromone
production are independent processes.
Long-distance attractants Pheromones are employed by a Sex attractant pheromones stimulate upwind flight by
large number of insects to bring the sexes together for members of the opposite sex bringing individuals of the
mating. These include sex attractant pheromones, pro- two sexes into proximity. In some cases, the sex attractant
duced by one sex and attracting the other, and aggregation odor appears sufficient to produce mating, but frequently
pheromones, commonly produced by one sex, but attract- vision or an odor produced by the opposite sex are impor-
ing individuals of both sexes. tant in the final stages.
Sex attractant pheromones are produced by the females Aggregation pheromones attract both sexes and, in
of some Homoptera, such as aphids and scale insects, by some cases also larvae. They are commonly associated with
many Lepidoptera and Coleoptera, and by some feeding behavior but also facilitate the meeting of the
Hymenoptera. Male ant lions (Neuroptera) are also known sexes. Bark beetles (Scolytidae) aggregate in large
to produce sex attractant pheromones. Amongst the cock- numbers on host trees selected for attack and many species
roaches (Blattodea), a sex attractant pheromone is produced are known to produce attractant pheromones. When a
716 CHEMICAL COMMUNICATION
Table 27.2. Sex attractant pheromones. Examples of chemicals which are commonly major constituents of the
pheromone in different families of insects. The term hydrocarbon is used here to refer to compounds with an unbranched
chain of carbon atoms.
Blattodea O O
O
Blattidae
cockroaches periplanones female atrial glands
H2 C
CH
periplanone - B
(CH 3 ) 2
O
Hemiptera
Aphididae terpenes O
female hind tibia
aphids
nepetalactone
O
CH 3 CH 2
C C C C C C
Diaspididae branched
scale insects C C C C O C female ?
hydrocarbons
3 - methylene, 7 - methyl,
7 - octen propanoate
O
Miridae C C C C
mirid bugs hydrocarbons C C C C
female ?
O
butyl butyrate
Neuroptera
Myrmeleontidae monoterpene
antlions + (see Fig. 27.6) male thorax
hydrocarbon
Hymenoptera CH 3 CH 3
Tenthredinidae C C C C C C C
branched
pine sawflies hydrocarbons C C C C C C male ?
OH
3,7 - dimethyl - 2 -tridecanol
O O
Apidae C C C C C
hydrocarbons female mandible
honeybees C C C C C OH
E 2, 9 - oxodecanoic acid
Trichoptera O
Rhyacophilidae C C C C
caddis flies hydrocarbons C C C C C female abdomen
nonan-2-one sternum 5
Lepidoptera
many families of moths hydrocarbons (see Fig. 27.7) female abdomen
intersegment 8-9
Coleoptera O
Scarabaeidae C C C C C C
scarab beetles hydrocarbons female ?
C C C C C C C C
Z - 7 - tetradecen - 2 - one
Scolytidae
terpenes see Figs. 27.8 and 27.13 both sexes ?
bark beetles
PHEROMONES 717
O
exo - brevicomin
mass attraction
of
both sexes
antiaggregation
pheromones
CH3 CH3 CH3 CH3
CH3 CH3
+
O OH
verbenone trans - verbenol
(from both sexes)
inhibit further
attraction
female Dendroctonus bores into the phloem of a host tree Hydropsyche, which forms male swarms, also produce an
she produces a pheromone, exo-brevicomin (Fig. 27.12) in aggregation pheromone with nonan–2-one as a major
the feces. It is attractive to both sexes and so more beetles component. Males of a number of Drosophila species
invade the tree. The males, when they arrive, produce a produce an aggregation pheromone consisting of a
closely related pheromone, frontalin, which, together with mixture of aliphatic hydrocarbons. This, acting together
the volatile myrcene from the tree itself, enhances the with odors from the habitat, attracts both sexes. It becomes
effect of the exo-brevicomin so that more and more beetles transferred to females during mating and the females then
arrive at the tree. As male beetles enter the female galleries transfer it to oviposition sites so that more insects are
they stridulate, leading to the release of pheromones which attracted (Hedlund et al., 1996).
reduce the attractant response. These ‘antiaggregative’ Gregarious locusts also produce aggregation
pheromones are trans-verbenol, verbenone and others. pheromones containing a number of aromatic hydro-
Aggregation pheromones are also produced by males carbons. Adults of both sexes as well as larval stages
of some scarab and nitidulid beetles, by some male weevils, produce the pheromone, apparently from the gut,
and by male Heteroptera from a number of families. In although there are some differences in the compounds pro-
many cases they are methyl branched hydrocarbons duced by adults and larvae (Torto et al., 1994).
(Aldrich et al., 1994; Bartelt, Weaver & Arbogast, 1995;
Hallett et al., 1995; James, Moore & Aldrich, 1994; Sex pheromones active at close quarters Many insects
Oehlschlager et al., 1995). Both sexes of the caddis fly, employ pheromones when the two sexes are in close
718 CHEMICAL COMMUNICATION
proximity. These may serve to identify the opposite sex female and induces her to mount on the male’s back.
with greater certainty and may also have the effect of Mechanoreceptors near the gland are stimulated when the
increasing the willingness of a female to mate. They are, female feeds indicating to the male that she is in the right
therefore, sometimes called aphrodisiac pheromones. position for mating (Farine et al., 1996).
They come into operation when the sexes have already Many cyclorrhaphan Diptera use cuticular hydro-
been brought together by some other signal, which may be carbons for sex recognition. These usually have chain
an attractant pheromone, a visual or mechanical stimulus, lengths of more than 25 carbon atoms and are often
or a common response to features of the habitat. methylated. They function as contact pheromones and,
Aphrodisiac pheromones are believed to be produced perhaps, as volatile attractants when the insects are already
by males of many Lepidoptera, although their presence is very close together. After mating, the composition of the
often inferred from the insects’ behavior rather than from female’s cuticular hydrocarbons changes, in Drosophila
the identification of the chemicals. In Danaidae, the males due to a change in synthesis, but in Glossina due to transfer
are visually attracted to the females and fly in pursuit. of cuticular components from the male. The effect of these
When a male Danaus gilippus overtakes a female he changes is to inhibit further courtship (Blomquist &
extrudes his hair pencils and dusts her with pheromone Dillwith, 1985; Howard, 1993).
transfer particles. These carry the pheromone which stim-
ulates the olfactory sensilla of the antennae and induce the Marking pheromones These pheromones are used by
female to land. The male may then hover over the female, social insects to define feeding or nest sites and to mark
continuing to dust her with pheromone particles, until trails. Amongst non-social insects they serve to mark posi-
finally he lands and copulates. The brushes of male tions occupied by eggs, or high densities of insects. They
Noctuidae are used in an essentially similar way, being might therefore be expected to be more persistent than
everted just before copulation when courtship is already in most other pheromonal signals and so to be less volatile.
progress. The associated release of pheromone is essential While this is sometimes the case, it is not always true; a lack
for copulation to occur. of persistence may sometimes be overcome by frequent
In Danaidae, the pheromones are derived from marking.
pyrrolizidine alkaloids taken up by the males (see Fig. Pheromones which cause the members of a population
27.8) and similar compounds are used by some male arctiid to become more widely spaced are sometimes called epi-
moths. Many noctuid moths employ mixtures of aromatic deictic pheromones. Females of many parasitic
hydrocarbons as aphrodisiac pheromones, but some other Hymenoptera and some phytophagous species of
families use aliphatic hydrocarbons or terpenoids. These Hymenoptera, Diptera and Lepidoptera, as well as some
compounds are produced in larger quantities than those beetles, mark their oviposition sites with a pheromone that
forming the attractant pheromones produced by females. often inhibits further oviposition in the same host or part
Males of some butterflies produce aphrodisiac of a plant (Table 27.3). These pheromones are called
pheromones from androconia on the wings. For example, in oviposition marking pheromones. In parasitic
Eumenis semele the male follows the female visually, and, ulti- Hymenoptera they are produced in Dufour’s gland, while
mately, if she is virgin, the female lands. The male has scent in the fruit fly, Rhagoletis, they are synthesized in the pos-
scales in a patch on the upper side of the fore wing (similar to terior midgut. The pheromones are deposited after
those shown in Fig. 27.10) and courtship is completed by the oviposition when the female drags the tip of her abdomen
male standing in front of the female and bowing towards her over and round the site. Few of these pheromones have
with the wings partly open so that the female’s antennae been identified. The principal component of that of the
come into contact with the scent areas. The female then ichneumonid wasp, Nemeritis, is heneicosane, the codling
allows the male to move round and copulate. moth, Cydia, uses a range of fatty acids with chain lengths
Glands which may produce aphrodisiac scents also of 14 to 18 carbon atoms, with linoleic acid (C18) being the
occur in various Neuroptera, Trichoptera, Diptera and most abundant (Thiéry et al., 1995), while the apple
Hymenoptera, sometimes in the male, sometimes in the maggot fly, Rhagoletis, produces taurine.
female. Some male cockroaches produce a substance from Epideictic pheromones are also produced by the larvae
a dorsal abdominal or thoracic gland which is fed on by the of some species. For example, the larvae of the flour moth,
PHEROMONES 719
Diptera HOCH2
O OH
Tephritidae O
midgut
Rhagoletis HO
fruit fly N - taurine
OH OH
Hymenoptera C C C C C C C C C C
Ichneumonidae C C C C C C C C C C C Dufour's
Nemeritis gland
parasitic wasp heneicosane
Lepidoptera C C C C C C C C
Tortricidae C C C C C C C C C C OH ?
Cydia O
codling moth linoleic acid
O OH
C
O
Pieridae HO
Pieris C N OH ?
cabbage butterfly HO
H
OH
miriamide
HO
O
Coleoptera
Anobiidae O
?
Lasioderma
cigarette beetle O serricorone
Ephestia, produce a pheromone from their mandibular and ants, social insects that forage on the ground, but a few
glands when they encounter other larvae of the same nonsocial insects, such as tent caterpillars, also produce
species. This pheromone causes increased wandering, them. The persistence of such trails depends on the
later pupation and ultimately results in smaller pupae. The number of individuals depositing the pheromone, the
moths emerging are consequently also smaller and, as nature of the pheromone, the substrate on which it is laid,
fecundity is proportional to size, fewer eggs are laid and and the prevailing environmental conditions. The trail laid
population density in the next generation is reduced. by a single ant is often relatively short-lived and it is only
Marking pheromones are also used by honeybees. The by constant reinforcement that more persistent trails are
secretion of the Nasonov gland is made up of seven different produced. Tent caterpillars lay a silk trail at the same time
terpenoids, including citral and geranic acid. The bees do not as their scent trail and the silk contributes to the ability of
deposit the pheromone on a surface, but worker bees expose the caterpillars to follow the trails.
the gland and disperse the scent by fanning with their wings. Termites produce a trail pheromone from a gland on
They exhibit this behavior at the nest entrance, guiding the ventral surface of the abdomen. In most species the
returning workers, and during clustering when a colony pheromone is produced continuously and a drop is
swarms. They may also occasionally use this pheromone to deposited each time the abdomen touches the surface. In a
guide other workers to sources of food or water. number of instances a constituent of the food forms one
Trail pheromones are another category of marking component of the pheromone system. In Coptotermes for-
pheromones. They are produced primarily by termites mosanus the major component of the trail pheromone is
720 CHEMICAL COMMUNICATION
Table 27.4. Trail pheromones. Examples of chemicals which are commonly major constituents of the pheromone in different
insects. Notice that different ant species (Formicidae) produce the pheromone in different glands.
Isoptera aliphatic
C C C C C ventral
Termitidae hydrocarbons
C C C C C C C OH abdominal
Coptotermes Z,Z,E - 3,6,8 - dodecatrienol gland
Lepidoptera ventral
Lasiocampidae steroids abdominal
Malacosoma (larva) gland
O
5β - cholestane - 3,24 - dione
O
CH 3
Hymenoptera N
Formicidae heterocyclic nitrogen poison
Ponerinae compounds O N gland
Megaponera CH 3
N,N - dimethyluracil
CH 3
Formicinae aliphatic C C C OH
O hindgut
Lasius hydrocarbons
hexanoic acid
Z,Z,E–3,6,8-dodecatrienol with Z,E,E–3,6,8-dodeca- Daceton can lay a trail using chemicals from the poison
trienol as a minor component (Table 27.4). gland or from the sternal gland. The trail produced by the
Ants lay scent trails which they use to mark foraging former is much more persistent, perhaps related to the
paths. The scent is produced in different glands in higher molecular weight compounds commonly produced
different subfamilies of ants and the products of one gland by the poison gland.
often differ between species. In many cases the pheromone Tent caterpillars lay trails by pressing the ventral
is a mixture of chemicals, perhaps giving specificity to the surface of the terminal abdominal segment against the
trail, and, in some species, the different chemicals may be substratum. If they find food, they overmark these
contributed by different glands. For example, workers of exploratory trails as they return to the nest and these trails
PHEROMONES 721
are then followed preferentially by other caterpillars. The monoterpenes, sesquiterpenes or short chain aliphatic
major components of the trail pheromone are two steroids, hydrocarbons, although other classes of compound are
and one, a monoketone, is more effective than the other, a produced by some ants (Table 27.5). These pheromones,
diketone, in inducing trail following. It is possible that the although commonly comprising mixtures of several com-
caterpillars modify the balance between these two chem- pounds, tend to be less specific than other types of
icals when laying different types of trail (Fitzgerald, 1993). pheromone. Alarm pheromones are commonly produced
Chemical trails are also utilized by some bees, though in the mandibular glands of social insects, although some
here the trail is followed in flight. In the stingless bees of species employ chemicals from other glands.
the genus Trigona a pheromone is used to mark the route to The effect of alarm pheromone in non-social insects is
a food source. A worker bee who has located a suitable food to cause dispersal. Aphids, for example, may fall from their
source marks it by biting and depositing the pheromone hostplant when they perceive the alarm pheromone.
from the mandibular glands. Further odor spots are made Amongst social insects, the response varies according to
at intervals of about 15 m back to the nest and recruited the species, but commonly involves attraction of other
workers follow the succession of odor spots to the food workers or soldiers and the adoption of aggressive pos-
source. Citral constitutes 95 % of the pheromone from the tures with the head raised and jaws wide apart.
mandibular glands of T. subterranea, but, in some other Different components of an alarm pheromone may
species, alcohols and ketones are amongst the major elicit different behavior in recipients and, because of their
constituents. different volatilities, and perhaps due to differences in the
Male bumblebees, Bombus, use marking pheromones sensitivity of the receiving insects, the areas over which
from the labial glands to mark out routes which they then they produce active responses by the ants vary (Fig. 27.13).
patrol. When it lands to mark, the bee grasps the object to For example, hexanal is the most volatile of the compo-
be marked in the mandibles and gnaws at its surface. The nents produced by Atta so the area over which it spreads
pheromone comprises a mixture of short-chain hydro- rapidly increases in size. It alerts the soldier ants, who raise
carbons and, in some species, monoterpenes (Bergman & their heads and open their jaws. Hexanol, the other major
Bergström, 1997). The mixture is species-specific and this component, is rather less volatile and spreads more slowly;
specificity is enhanced by the tendency of different species at low concentrations it stimulates movement towards the
to mark different objects and to fly at different heights site of release. Other compounds are present in small
(Appelgren et al., 1991). Each time a male comes to a quantities and are effective only close to the point of
marked point he hovers for a short period before flying on deposition. This is true of both 3-undecanone and 3-
to the next point. The function of these routes is not clear butyl–2-octenal which both induce biting.
although it is assumed that they facilitate mate finding. The alarm pheromone of the bee Trigona is also pro-
Comparable scent routes are also made by males of some duced by the mandibular glands. At least some of the
other bees such as Psithyrus and Anthophora. chemicals which are used in trail-laying also function in
The importance of chemical mixtures in conferring producing alarm, the nature of the response depending on
specificity to the signals provided by pheromones is illus- the situation. An alarm pheromone is produced in the
trated by members of the genus Trigona. Trigona postica is mandibular glands of Apis, and another is released via the
unable to follow the trails of either T. spinipes or T. xan- sting chamber. Guard bees at the entrance to a hive use this
thotricha, but T. xanthotricha can follow the trail of T. to mark intruders and to stimulate aggressive activity by
postica. All these species produce 2-heptanol as a major other bees.
component of the trail pheromone, but in T. spinipes there Reviews: Aldrich, 1995 – heteropteran secretions; Birch, Poppy
are only three known components compared with at least & Baker, 1990 – male moth pheromones; Blum, 1985 – alarm
ten in the other two. pheromones; Boppré, 1984 – male moth pheromones; Borden,
1985 – aggregation pheromones; Haynes & Birch, 1985 – trail
Alarm pheromones Alarm pheromones are produced as a pheromones; Pickett et al., 1992 – aphid pheromones;
response to disturbance by some Thysanoptera and Prokopy, 1981 – spacing pheromones; Tamaki, 1985 -sex
Hemiptera that tend to feed in groups and also by social pheromones; Traniello & Robson, 1995 – trail pheromones of
insects. They are usually highly volatile compounds, social insects
722 CHEMICAL COMMUNICATION
Table 27.5. Alarm pheromones. Examples of chemicals which are commonly major constituents of the pheromone in
different families of insects. The term hydrocarbon is used here to refer to compounds with an unbranched chain of
carbon atoms.
Isoptera
Termitidae terpenes cephalic
gland
limonene
Thysanoptera C C C C C O CH 3
Thripidae hydrocarbons C C C C C C ?
decyl acetate O
Hemiptera CH 3 CH 3 CH 2
Aphididae C C C C C C cornicles
terpenes
C C C C C C
E - β - farnesene
C C C
Tingidae hydrocarbons C C C H dorsal abdominal
E 2 - hexenal gland
O
+
OH
monoterpenes
geraniol
C C C
Coreidae hydrocarbons C C C H metathoracic
hexanal gland
O
Hymenoptera O
worker Nasonov
gland
mandibular tarsal
glands poison glands
gland
orientation
outside attraction to
effects on to aggressive behavior colony,
colony workers swarm leading to stinging foraging site,
swarm
effects on attraction
drones
queen
mandibular tergal
glands tarsal gland
glands
pheromone brood
pheromone
larva
their antennae and tongues resulting in the transfer of the bees produce queen substance in the mandibular glands,
pheromone to their bodies. Transfer through the colony workers produce 2-heptanone, an alarm pheromone. In
results from the frequent contacts made by these workers the leaf-cutting ant, Atta sexdens, minor workers whose
with others. One major function of the pheromone is to principal duties are within the nest, produce the same
inhibit the development of the workers’ ovaries (Fig. chemicals in their mandibular glands as sexual males and
27.14), but it also inhibits queen rearing by the workers. females. Major workers, engaged in foraging, and soldiers,
Different castes produce different pheromones even with a defensive role, have completely different major
from the same glands. For example, while queen honey- components (Fig. 27.15).
SECRETIONS WITH INTERSPECIFIC SIGNIFICANCE 725
C C C
27.2.1 Structure and distribution of glands
4 - methyl - 3 -
C C C C heptanone Glands involved in producing chemicals for interspecific
O signalling in general differ from pheromone glands in
CH 3
having a reservoir in which the chemicals are stored; the
C C C 4 - methyl - 3 -
C C C C heptanol quantities of chemical involved are much greater than
OH those employed as pheromones. Most defense glands
develop as invaginations of the epidermis and are lined by
CHO geranial cuticle, the obvious exception being those salivary glands
which produce defensive substances. The glands can be
CHO grouped into those which are not everted, but from which
neral
the chemicals are expelled, sometimes forcibly, and those
which can be everted and from which chemicals diffuse
away or are effective only on contact.
Fig. 27.15. Caste differences in mandibular gland secretions of
the leaf-cutting ant, Atta (based on Nascimento et al., 1993). Non-eversible glands In non-eversible glands, the gland
cells may line a reservoir, or the secretory region and reser-
voir may be separate and joined by a duct. The gland cells
Kin recognition is an important aspect of social insect usually have ducts leading through the cuticle (class 3 cells),
behavior both with respect to recognizing members of but in the prothoracic glands of notodontid larvae they do
other colonies and in recognizing brood. Colony recogni- not (class 1 cells). The reservoir is lined by cuticle and its
tion probably often involves innate characteristics together opening to the exterior is normally closed by the elasticity of
with acquired environmental characters. Both are learned the surrounding cuticle and opened by specific muscles.
by the individual insects when they eclose. Differences Exocrine glands producing chemicals that are known or
between colonies in the composition of cuticular waxes presumed to have an interspecific role are known from
have been demonstrated in some social wasps and ants, species in almost all orders of insects except for the
providing a basis for colony recognition (Layton, Camann Phthiraptera and Siphonaptera, which are parasitic on ver-
& Espelie, 1994). In Apis colonies, small differences in cut- tebrates, and for Thysanura and Mecoptera. Their posi-
icular hydrocarbons also exist between individuals that are tions and form are very variable, but within a particular
full sisters, having the same father, and half sisters, having insect group they are more uniform. A few examples are
different fathers; individual bees can discriminate between given to illustrate the variety of structures. The soldiers of
the two. Rhinotermitidae and Termitidae have a gland called the
Recognition of brood by adult social insects depends frontal gland which discharges its secretion through a
largely on the presence of pheromones on the larval median anterior pore in the head. In some rhinotermitids
cuticle. the reservoir is extremely large and occupies more than half
Reviews: Hölldobler & Wilson, 1990 – ant pheromones; Smith & the abdominal cavity, but in termitids it is restricted to the
Breed, 1995 – social recognition; Winston, 1987 – honeybee head capsule. Nasute termites have the front of the head
pheromones; Vander Meer et al., 1998 – social insects modified to form a rostrum with the gland opening at the
726 CHEMICAL COMMUNICATION
opener
muscles
reservoir
tergite 4
dorsal
glands
tergite 5 gland cells stretch
muscles
b) separate reservoir
transverse section
of gland gland
cell
gland
collecting
canal
transverse section
of reservoir
reservoir
lumen
pygidial
gland tergum 8
opening of reservoir cuticle
beneath tergum
tergum 9
Fig. 27.16. Non-eversible exocrine glands. (a) Gland cells directly associated with reservoir. Abdominal glands of larval
Heteroptera, Pyrrhocoris (after Staddon, 1979). (b) Gland cells separate from reservoir. Coleopteran pygidial gland, Cicindela
(based on Forsyth, 1970).
tip. The soldiers of some Termitidae have the salivary inside the metathoracic and second abdominal spiracles,
glands modified for defense, the reservoir occupying the respectively. In the grasshoppers, the secretion is stored in
front half of the abdomen, with the secretion being ejected the trachea which is not normally used in respiration.
from the mouth as a result of abdominal contraction. Heteropteran larvae typically have glands in the dorsal
The romaleid grasshoppers and a cockroach, abdomen opening behind the tergites, usually by a single
Diploptera, have glandular epithelium lining a trachea median pore (Fig. 27.16a). Sometimes they occur in
SECRETIONS WITH INTERSPECIFIC SIGNIFICANCE 727
segments 3 to 6, but often they are reduced in numbers. 27.2.2 Storage within the body
They sometimes persist in adults, which also typically Chemicals used in interspecific communication are often
have a ventral metathoracic gland. This is often complex stored within the body, as well as, or instead of, in glands.
with lateral and median reservoirs which open via lateral Fig. 27.18 shows the distribution of ouabain, a cardiac gly-
ducts between the meso- and metathoracic legs. It exhibits coside, in the adult of the milkweed butterfly, Danaus plex-
great variation between species and is often reduced in ippus. About 80% is in the integument of the wings and the
species that sequester chemicals from plants. rest of the body, but an appreciable amount is in the fat
Nearly all adephagan beetles have a pair of pygidial body.
glands, in which the secretory lobes are distinct from the The integument is a storage site for cardiac glycosides
reservoirs, opening behind abdominal tergite 8 (Fig. in the milkweed bug, Oncopeltus, and in Danaus plexippus;
27.16b). Adult chrysomeline beetles have glands opening for cyanogenic glycosides in the larva and adult of the
on the pronotum and the elytra (Fig. 27.17). In this group, burnet moth, Zygaena; and quinolizidine alkaloids in the
there are many separate glands which have no reservoirs. caterpillar of Uresiphita. In larval Zygaena, there are large
Instead, the secretions are stored in vacuoles and in extra- cavities in the cuticle of the meso- and metathorax and of
cellular spaces. Many other groups of beetles also have the first eight abdominal segments in which the glycosides
exocrine glands with a probable defensive function are stored (Fig. 27.19a). Smaller cavities are present in the
(Dettner, 1987). rest of the cuticle of the dorsal and lateral regions of the
Amongst Lepidoptera, larval Notodontidae have a body. In Oncopeltus, there is a layer of vacuolated cells
gland opening ventrally in the neck membrane. The gland immediately beneath the epidermis over much of the
is single-chambered in some species, but has two chambers thorax and abdomen (Fig. 27.19b).
in others (Attygalle et al., 1993). Storage in the hemolymph occurs most frequently
728 CHEMICAL COMMUNICATION
hemocoel
cuticle
epidermis
cell of inner
layer
vacuole containing
cardiac glycosides
basal
lamina
exocrine glands of some water beetles contain a range of chrysomelid beetles, several lepidopteran species, and a
sesquiterpenes, while some staphylinid beetles produce grasshopper, Zonocerus, sequester alkaloids from their host
citral in their abdominal glands. plants.
Steroidal compounds, with a presumed defensive func- A number of Lepidoptera contain cyanogenic com-
tion, are present in the bodies of insects from several orders. pounds including the glycosides linamarin and lotaustralin
The grasshopper, Poekilocerus, has cardiac glycosides in the from which hydrogen cyanide may be produced. A few
secretion of its dorsal thoracic gland. Cardiac glycosides are beetles also contain cyanogenic glycosides.
also sequestered in the integument of the milkweed bug and Biogenic amines and proteins are also secreted by some
the milkweed butterfly and are synthesized by some insects. An amide, pederin, is produced by some
chrysomelid beetles where they are present in the hemo- staphylinid beetles (Kellner & Dettner, 1995). Pompilid
lymph. and sphecid wasps produce histamine and 5-hydroxy-
Alkaloids are synthesized or sequestered by a variety of tryptamine, and sometimes also acetylcholine, in their
insects. For example, unique alkaloids, produced by the poison glands. Peptides known as melittins constitute
insects, are present in the hemolymph of coccinellid about 50% of the dry weight of bee venom, and other pep-
beetles and the venom of fire ants, Solenopsis, and tides are present in smaller amounts. The venom of bees
Pharaoh’s ant, Monomorium. On the other hand, some and some ants also contains several enzymes:
730 CHEMICAL COMMUNICATION
hyaluronidase, phospholipase and phosphatase. Tent The amounts and particular chemicals sequestered are
caterpillars and adults of some moths, like Euproctis have affected by differences in the food (Fig. 27.21), and the
specific proteins associated with urticating hairs. quantities may be very large. For example, the iridoid gly-
In addition to these major classes of substances which cosides sequestered by the checkerspot butterfly,
are commonly identified in known or supposed defensive Euphydryas, may constitute 10% of the insect’s dry
secretions, insects produce a variety of chemicals belong- weight.
ing to other chemical classes. In a few cases, chemicals are separated from the food
Reviews: Aldrich, 1988 – Heteroptera; Brower, 1984 – during ingestion. Larvae of the sawfly, Perga, feed on
butterflies; Davis & Nahrstedt, 1985 – cyanogenesis; Dettner, Eucalyptus. Oils from the food are sequestered in a diverticu-
1987 – Coleoptera; Piek, 1985 – Hymenoptera; Prestwich, 1984 – lum on the ventral side of the foregut; very little oil reaches
Isoptera the midgut and in the last stage larva the full gland may make
up 20% of the body weight. Similar adaptations occur in
27.2.4 Origins of chemicals larvae of Neodiprion feeding on Pinus and in larvae of
Many chemicals are synthesized de novo by insects, but Myrascia (Lepidoptera) feeding on Myrtaceae (section 3.1.1).
many plant-feeding species sequester chemicals from their Reviews: Blum, 1987 – synthesis; Bowers, 1990 – sequestration;
hosts. Some insects are able to synthesize as well as Duffey, 1980 – sequestration
sequester some chemicals.
27.2.5 Avoidance of autotoxicity
Synthesis Synthesis of interspecific signalling chemicals is A critical problem for insects that produce or sequester
of widespread occurrence in insects. This applies not only chemicals that are potential toxins is the avoidance of auto-
to relatively simple structures like aliphatic hydrocarbons toxicity. Two processes contribute to this: first, the insects
and monoterpenes, but to some much more complicated may exhibit some degree of tolerance to the toxins, and
structures. For example, cardiac glycosides are synthesized second, the enzymes and substrate producing a toxin may
by some chrysomelid beetles, and alkaloids by coccinellid be in separate compartments so that synthesis only occurs
beetles and fire ants. Insects with this capacity produce the outside the body.
same suite of compounds irrespective of their food. Cardiac glycosides are toxic to animals because they
inhibit the enzyme Na⫹/K⫹-ATPase, but in insects that
Sequestration Many plant-feeding insects sequester plant sequester these compounds, this enzyme is 100 times less
toxins which often are not secreted to the outside, but are sensitive to inhibition than in some other, susceptible,
retained within the body so they are effective only when insects. In Danaus plexippus this insensitivity results from a
the insect is tasted by a predator. The species which do this change in a single amino acid on a binding site of the
are often specialists on plants containing specific classes of enzyme (Holzinger & Wink, 1996).
chemical, presumably reflecting the ability of the insects to Insects that store cyanogenic glycosides in the cuticle
tolerate high concentrations of the particular chemicals. are also less sensitive to cyanide poisoning than most other
An exception to this generalization is the lubber grass- organisms, although the mechanism of resistance is not
hopper, Romalea, which feeds on many different plants known. Zygaenid larvae have a -glucosidase, with high
and sequesters a range of different chemicals. specificity for the glycosides, in the hemolymph. Cyanide
Compounds commonly sequestered are cardiac and is produced only if the cuticle is punctured, so that hemo-
iridoid glycosides, cucurbitacins and pyrrolizidine alkaloids lymph and glycosides come together.
(Table 27.6). Sequestration is selective and compounds may Quinones are often produced outside the body. For
be stored unchanged or after some reconstruction. For example, the quinones produced by tenebrionids are prob-
example, Euphydryas sequesters some iridoid glycosides ably derived from phenol glucosides by hydrolysis fol-
unchanged, others are metabolized before storage, and lowed by oxidation. These processes may take place in the
others are excreted (Fig. 27.20). The larvae of Danaus plex- end-apparatus of the secretory cells, which is extracellular.
ippus selectively store polar cardiac glycosides, but excrete An extreme example of the extracellular production of
those that are apolar. Some chrysomelid beetles synthesize the active component occurs in bombardier beetles.
salicaldehyde from salicin in their food. Quinones are generated explosively by the oxidation of
SECRETIONS WITH INTERSPECIFIC SIGNIFICANCE 731
CH 3 O
O Poekilocerus bufonius (Orthoptera)
cardiac glycosides HO Asclepiadaceae Aphis nerii (Hemiptera)
OH C
O
Oncopeltus fasciatus (Hemiptera)
Danaus plexippus (Lepidoptera)
OH
CH 3 O O
calotropin
OH
CH3 CH3
CH
Zonocerus variegatus (Orthoptera)
pyrrolizidine alkaloids HO CH2 O CO C CHOH CH3 Asteraceae Tyria jacobaeae (Lepidoptera)
Oreina cacaliae (Coleoptera)
OH
O COOH
NO2
O
isoquinoline alkaloids Aristolochiaceae Battus philenor (Lepidoptera)
OCH3
aristolochic acid
O
H3 C
HO
CH 3 O
CH 3
O O C
CH 3
triterpenoids CH 3 Cucurbitaceae Diabrotica undecimpunctata (Coleoptera)
HO
CH 3
CH 3
O
cucurbitacin B
CH 3 CH 3
hydroquinones so that they are ejected as a spray through 27.2.6 Dispersal of chemicals
the openings of the pygidial glands. The hydroquinones Dispersal of the chemicals from the glands depends on the
are stored with hydrogen peroxide in the glands, but at the opening of the ducts leading to the exterior which are held
moment of discharge these chemicals are mixed with cata- closed by the elasticity of the cuticle. This is achieved by
lases and peroxidases from an accessory chamber. This opener muscles. Where the gland is surrounded by a
causes the sudden decomposition of the hydrogen per- muscle layer, as in the stick insect, Extatosoma, and the
oxide and oxidation of the hydroquinones so that the pygidial glands of adephagan beetles, muscle contraction
quinones are forcibly ejected with an audible explosion and forces the secretion through the ducts to the outside. In
the generation of temperatures up to 100 °C. other cases, contraction of body wall muscles acting on the
732 CHEMICAL COMMUNICATION
isovanillylcatalpol
excreted unchanged
mussaenoside
OH R1
OC R2
verproside
R1 = OH R 2 = H
aucubin
O O
veronicoside
HOH2C O glucose R1 = H R 2 = H
O
O isovanillylcatalpol
OH HOH2C O glucose R1 = OH R 2 = OCH 3
catalpol
O COOCH3
O H
HOH2C O glucose
mussaenoside
O
HO CH3 O glucose
gland via the hemolymph leads to compression of the compressing the abdomen to force air through the secre-
gland. Eversible glands are also inflated by hemolymph tion in the metathoracic trachea.
pressure. A few species have special applicators with which they
In some cases, compression of the reservoir is so rapid apply chemicals to surfaces. For example, some vespid
that fluid is forcibly ejected, in several cases travelling up wasps have a gland, known as van der Vecht’s gland, with
to 20 cm from the insect. Sometimes the ejection is accom- ducts opening along the anterior edge of the sixth abdomi-
panied by behavior that directs the spray towards the nal sternite. Hairs surrounding the openings are used as a
aggressor. Notodontid larvae, for instance, raise the front brush to apply the repellent contents of the gland to the
half of the body and turn to face the potential danger pedicel supporting the nest (Dani, Morgan & Turillazzi,
before they spray. Parachartergus colobopterus, a small 1995).
social wasp, directs a spray of venom from its poison gland The hairs of some urticating caterpillars and moths can
at a source of disturbance by twisting its gaster so that it penetrate the skin of vertebrates and so deliver their toxins
points forwards (Jeanne & Keeping, 1995). A few grass- subcutaneously. Tent caterpillars have eight tufts of
hoppers with dorsal glands also eject a spray. barbed hollow hairs associated with the glands producing
Romaleid grasshoppers that have glands associated urticating substances, while some moths have a dense
with a trachea emit a frothy bubble of chemicals from the abdominal brush of hairs with holes at the tips through
metathoracic spiracles by closing all the other spiracles and which, it is presumed, their urticating protein is delivered.
SECRETIONS WITH INTERSPECIFIC SIGNIFICANCE 733
locality
B O
1500 1985
locality
dry weight (µg)
A
1000
1985 locality
1986 C HO
1986
500 H
1986
Fig. 27.22. A tetracyclic diterpene that contributes to the glue
0 secreted by soldier Nasutitermes.
aucubin catalpol
Fig. 27.21. Sequestration. Variation in total amounts and relative mutualistic relationships. Compounds may have more
proportions of different iridoid glycosides sequestered by male than one function.
Euphydryas anicia from different localities and different years.
Insects at locality C also sequestered a small proportion of a third Defense against predators Enemies may be incapacitated
glycoside, macfadineoside, that was not present in insects from by the physical nature of some secretions. The secretion of
the other populations (indicated by the thicker black line at the the frontal glands of nasute termites hardens to a sticky
top of the bar for 1986) (based on Gardner & Stermitz, 1988; thread in air due to the presence of oxygenated diterpenes
L’Empereur & Stermitz, 1990).
(Fig. 27.22). It is ejected on contact with predators such as
ants, and its irritant action, which results from the pres-
Where the chemicals are volatile, the cuticle outside the ence of monoterpenes, causes the ant to preen, spreading
gland opening may be highly sculptured, perhaps to facili- the entangling material even more. The ant may die if it is
tate evaporation. Over most of the osmeterium of papil- unable to free itself of the sticky substance. Some com-
ionid caterpillars, the cuticle is produced into numerous pounds of the secretion also act as an alarm pheromone
papillae which hold the secretion when the gland is invagi- attracting other termite soldiers from up to 30 cm away. In
nated and facilitate evaporation when it is expanded. Macrotermes subhyalinus, on the other hand, the frontal
Where chemicals are stored in the cuticle, they may be gland secretion of the soldiers apparently kills ants by pre-
present on the surface so that they directly affect potential venting wound healing following a bite. The oily secretion
predators. A larval zygaenid compresses its body when oozes from the gland and coats the surface of the termite’s
attacked so that bubbles of fluid containing cyanogenic head and is transferred to the enemy during combat.
glycosides are forced out from the reservoirs, rupturing Repellent effects of sprays are recorded in a number of
the cuticle at points of weakness at the bases of the exit insects. Anisomorpha directs the spray from its thoracic
pores. When the insect relaxes, the bubbles are withdrawn. glands at enemies. Predatory ants and beetles elicit this
In Oncopeltus, cardiac glycosides from the subepidermal response if they bite any part of the stick insect; but blue
reservoirs are also forced through weak points where the jays are sprayed before they touch the insect and a single
cuticle is much thinner than elsewhere. Insects with com- experience is sufficient for a bird to learn to avoid the insect
pounds stored in the hemolymph exhibit reflex bleeding. subsequently. An adult female Anisomorpha can produce
They have points of weakness in the membranous cuticle, up to five discharges in a short time, but it then takes up to
often at joints in the legs, through which they are able to 15 days for the store of deterrent to be replenished; when
force drops of hemolymph. its store is depleted it is susceptible to attack. The secre-
tions of Poekilocerus, which can be ejected for up to 40 cm,
27.2.7 Interspecific functions of chemicals are also effective in repelling vertebrate predators. In this
The main functions of these chemicals are the incapacita- insect, too, the store of repellent is exhausted after about
tion or repulsion of potential parasites or predators, prey five expulsions.
capture, and protection against micro-organisms. In a Many insects produce secretions in response to an
few cases, the chemicals are essential components of immediate attack, but the volatility of the chemicals may
734 CHEMICAL COMMUNICATION
insects (%)
27.5). In the Hymenoptera, larvae of the sawfly,
Neodiprion, emit a drop of fluid from the foregut reservoir 50 0.5
when attacked. The fluid remains on the mouthparts and
repels ants and birds from a distance. Similarly, the alkaloid
Table 27.7. Antibiotic effects. Phenolic compounds known to have antibiotic effects that
occur in the secretions of insects.
Hemiptera
metathoracic
Notonectidae gland
Notonecta CH
O
p - hydroxybenzaldehyde
OH
Hymenoptera
metapleural
Formicidae gland
CH3 CHCH2CH3
Crematogaster
CH3
3 - pentylphenol
Atta metapleural
gland
CH2 COOH
phenylacetic acid
Coleoptera
Dytscidae N pygidial gland
COOCH3
Ilybius OH
methyl 8-hydroxyquinoline-2-carboxylate
benzoic acid
ganglia. Ampulex compressa (Sphecoidea) makes two injec- as philanthotoxin, which causes a neuromuscular block by
tions, the first into the prothorax and the second into, or blocking glutamate receptors (Fig. 27.24). The venoms of
near, the subesophageal ganglion of a cockroach. The first some species affect a wide variety of prey species, but in
injection has a short-lived paralysing effect on its prey; the other cases they appear to be relatively specific, so that
second is irreversible. The prey is still able to walk and the injection into an inappropriate species has no effect.
venom does not affect either sensory input or motor output, Many parasitic Hymenoptera, such as Braconidae,
but has a neuromodulatory effect at specific synapses within Ichneumonidae and Chalcididae, also use a venom which
the thoracic ganglia (Fouad, Libersat & Rathmayer, 1996). serves to immobilize the host. This is true even of species
The principal constituents of the venom and their which lay their eggs on the outsides of their hosts. The
effects on the prey differ from species to species. effect is often to cause a partial and temporary paralysis of
Histamine, acetylcholine and serotonin (5-hydroxytrypta- the host while the insect is ovipositing. The venom is fol-
mine) are present in the venoms of some species. The lowed, in some species where the larvae are internal para-
venom of Philanthus triangulin (Sphecoidea), which preys sites, by fluid from the calyces of the oviducts which, in
exclusively on bees, contains a specific compound known some species, contains a polyDNA virus (section 5.3.4).
736 CHEMICAL COMMUNICATION
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Taxonomic Index
Page numbers in bold denote illustrations. The major orders are omitted.
Bledius, 488 Cerambycidae, 57, 87, 370 Collembola, 8–9, 11–12, 31, 134, 151–2, 168,
Blepharoceridae, 264, 381, 393, 469 Ceratitis, 311 172, 174, 263, 273, 277–8, 281, 334, 429,
Bolitophilidae, 674 Ceratocystis (fungus), 84 443, 449, 452, 478, 495, 551, 574, 587, 591,
Bombus, 23, 203, 250, 302, 510–12, 517, 604, Ceratopogon, 180–1 674
721 Ceratopogonidae, 16, 20, 23, 381 Coloburiscoides, 480
Bombycoidea, 194, 380, 588 Cercopidae, 170, 501 Columbicola, 60, 495
Bombyliidae, 371 Cerura, 267, 380, 391, 662, 667–8 Coniopterygidae, 280
Bombyx, 34, 53, 59, 69–72, 89, 95–6, 104–5, Chaetophyes, 501 Conocephalus, 683
108–10, 114, 122, 136, 198, 276, 284–5, Chalcididae, 192, 735 Copidosomopsis, 355
290–1, 304, 317–18, 326, 345, 357, 392, Chalcidoidea, 186, 314, 379 Coptotermes, 719–22
404–6, 408,449, 453, 524–5, 571–2, 636, Chaoborus, 95–6, 179, 181, 473 Coranus, 687
638, 668, 713 Charagia, 193 Cordylobia, 473
Bootettix, 376 Chilo, 74, 314, 365–6 Coreidae, 328, 722
Brachycera, 17, 277, 370 Chironomidae, 126, 381, 620, 666 Corioxenos, 372
Braconidae, 126, 735 Chironomus, 109, 115, 126, 135, 317, 319, Corixa, 621
Brsssicaceae (plant), 18 393, 464, 473–4 484, 487, 491, 663 Corydalis, 98, 469
Bruchidius, 65 Choristidae, 193 Costelytra, 711
Buenoa, 134, 684 Chorthippus, 287, 289, 331, 629, 686, 693–5, Cotesia (=Apanteles), 124, 126, 312, 472–3
Buprestidae, 370, 658 698 Creatonotus, 714
Chortoicetes, 205, 331 Crematogaster, 735
Calandra, 87, 333 Chortophaga, 271, 276 Crocothemis, 279
Calliphora, 32–3, 47, 105, 110–11, 120–1, Chrotogonus, 192 Cryptocercus, 56, 85, 519
132, 156, 196, 201, 216, 218, 220, 222–3, Chrysobothris, 483 Cryptochaetum, 472
235, 277, 295, 326, 328–9, 333, 363, 390–2, Chrysogaster, 461 Ctenolepisma, 60, 338
426, 432, 441, 454–5, 486, 501, 545, 551, Chrysolina, 728 Cucurbitaceae (plants), 731
579, 599, 611, 620 Chrysomelidae, 342, 351, 379 Culex, 69, 75, 78, 86, 330, 347, 349, 487, 580,
Calliptamus, 265 Chrysomya, 311 644
Callosobruchus, 325, 328 Chrysopa, 70–1, 317, 335, 501, 621–2, Culicidae, 18, 23, 44, 190–1, 277–8, 381, 393,
Calopteryx, 187, 469 626 462, 620–1
Calosoma, 259, 261 Chrysoperla, 620, 681 Culicoides, 311, 639
Calpodes, 111, 120, 132–6, 269, 275, 422, 429, Chrysopidae, 698 Curculionidae, 191, 685
431–3, 435, 501 Chrysops, 406, 555 Cychrini, 52
Camnula, 330 Cicadellidae, 170, 696, 698 Cyclochila, 688–9
Campodea, 263, 281–2, 495 Cicadidae, 231, 621, 680, 686 Cyclorrhapha, 15, 196, 338, 346–8, 370, 375,
Campodeidae, 262 Cicindela, 604, 606–7, 726 428–9, 432, 501, 605
Camponoti, 87 Cicindelidae, 25, 621, 658 Cydia (=Laspeyresia), 521, 718–19
Camponotus, 521, 588, 596–7, 726 Cimex, 24, 51, 108, 287, 311, 363–5, 526, Cylas, 54
Canace, 470 573 Cyllecoris, 367
Carabidae, 159, 191, 363, 588, 685, 728 Cimicidae, 85–6 Cynipidae, 358, 393
Carabini, 52 Cimicoidea, 287, 313, 328 Cynodon (grass), 90
Carabus, 492 Cimicomorpha, 314, 327, 363, 684 Cyrtacanthacridinae, 288
Caraphractus, 180 Clitumnus, 117 Cystosoma, 687–8, 695, 697
Carausius, 107–8, 155, 160, 162, 235, 306, Cloeon, 94, 196, 468, 590
326, 346, 357, 478, 493–4, 486, 488, 501, Clusiidae, 173 Daceton, 720
525, 541, 572, 576, 617, 665, 667, 670 Clytra, 337–8 Dactylopius, 663
Caryedes, 483 Coccidae, 357, 380, 382, 707 Dacus, 309, 333–4, 336, 339, 363, 686
Cassidinae, 320, 658, 666 Coccinella, 521, 673 Danaidae, 666, 718
Cataglyphis, 457, 523, 600–1 Coccinellidae, 591 Danainae, 714
Cavariella, 645 Coccoidea, 368, 663, 666 Danaus, 60, 291, 369, 505, 673, 712, 718,
Cecidomyiidae, 83, 351, 355, 358 Coccygomimus, 313 727–8, 730–1
Celithemis, 230 Cochliomyia, 70–1, 76, 78 Decticus, 238, 249, 622, 624
Cenocorixa, 478, 480 Coelopa, 487 Deilephila, 597
Centris, 290 Coenagriidae, 279 Delia, 289–90
Cephus, 407, 521 Colias, 511, 514, 674 Delphacidae, 85, 696, 698
TAXONOMIC INDEX 743
Musca, 15, 82, 95, 174, 260, 290–1, 314–15, 270, 273, 277–9, 299, 314, 336, 339, 356, Periplaneta, 9–10, 20, 35, 39–40, 51, 60, 74,
326, 329, 351, 371, 453, 486, 501, 636 363, 367, 378, 393, 417, 454, 465, 478, 482, 78, 85, 95, 97–8, 102, 104–6, 108, 110,
Muscidae, 244, 259 501, 551, 591, 599–600, 604, 619, 662, 114–15, 119, 153–6, 160, 162, 164–8, 230,
Muscoidea, 328 666–7, 674, 686 233–5, 238, 248–9, 265, 270, 295, 312, 320,
Mutillidae, 192 Odontomachus, 25, 708 352, 373, 451, 454, 458–9, 478, 481–3, 492,
Mycetophilidae, 24, 277 Odontotermes, 728 500, 522, 524–8, 541, 547, 549–51, 558,
Mymaridae, 191 Oecanthus, 342, 682, 695, 700 561, 565, 575, 599–600, 602, 619, 642–3,
Myrascia, 38, 40, 730 Oecophylla, 34, 357 646, 705
Myrmecaphodius, 736 Oedaleus, 79 Perla, 149
Myrmecocystus, 34 Oedipoda, 623, 681 Petrognatha, 459
Myrmeleon, 108, 710 Omocestus, 695 Petrobius, 314, 576
Myrmeleontidae, 24, 190, 716 Oncopeltus, 32–3, 35, 52, 76, 118–19, 269, Phasmatodea (=Phasmida), 95–6, 108, 162,
Myrmica, 688, 706 279–80, 287, 308, 328–9, 349–50, 365, 327, 345, 373, 375, 574
Myrmicinae, 686, 720, 722 377, 395, 505, 673, 727, 729, 731, 733 Phasmida, see Phasmatodea
Myrtaceae (trees), 38, 730 Onychiurus, 674 Phausis, 677
Myzus, 70–1, 88, 266, 520–1 Onymachus, 106–7 Pheidole, 401
Onymacris, 115–16, 489, 492, 494–6 Phengodidae, 674
Nabidae, 52 Oodes, 266 Philanisus, 500
Nasonia, 325, 357, 406 Operophtera, 517–18 Philanthus, 26, 735–6
Nasutitermes, 733 Opifex, 491 Philonthus, 157
Naucoris, 5, 464, 469 Orchestes, 169 Philosamia, 223, 229, 391
Nauphoeta, 31, 290, 395 Oreina, 731 Philotermes, 736
Nematocera, 45, 269, 280, 285, 334, 342, 363, Orgyia, 124, 126, 386 Phlebotomus, 297
370, 379, 391, 574, 620 Orius, 268–7 Phlogophora, 715
Nemeritis, 718–19 Orneodidae, 191 Phonoctonus, 673
Nemestrinidae, 371 Ornia, 629 Phormia, 51, 64, 69–71, 76, 80, 82, 114, 245,
Nemopteridae, 192 Ornithacris, 336, 350 295, 306–7, 391, 495, 646, 648–9, 651
Nemoria, 90, 403 Orthorrapha, 379, 574 Photinus, 676–7
Neoconocephalus, 231, 250, 510, 684, 693 Oryctes, 60, 109, 127, 204, 238 Photuris, 589, 674–7
Neodiprion, 38, 371, 521, 730, 734 Oryzaephilus, 671 Phrixothrix, 676
Nepa, 327, 331, 616 Osphya, 278 Phrynocolus, 492
Nephotettix, 696 Ostrinia, 10, 325, 349, 705 Phthiraptera, 60, 85, 95, 192, 268, 273, 300,
Nepidae, 157, 325–6, 329, 462 Otiorrhynchinae, 393 327, 338, 346, 373, 523, 587, 725
Nesomachilis, 263 Otiorrhynchus, 357 Phyllodecta, 519
Neuroterus, 358 Oxycheila, 685 Phyllopertha, 330–1
Nicrophorus, 701 Phymatidae, 157
Nilaparvata, 28, 696, 698 Pachycondyla, 706, 714 Phytobius, 469
Noctuidae, 686, 705, 708, 711, 714, 718 Paederus, 728 Pieridae, 10, 381, 660–1, 666, 719
Noctuoidea, 621–2 Panicum (grass), 90 Pieris, 19, 29, 57, 65, 81, 102, 106, 325, 363,
Nomadacris, 106, 147, 260, 265, 371 Panorpa, 195, 278 382–4, 405, 458, 482, 484, 486, 489, 521,
Nomuraea (fungus), 114, 123 Panteophylus, 684 555, 630–1, 648–51, 671, 719
Notiphila, 461 Papilio, 187, 207, 519, 607, 645, 667, 673 Pimpla, 317
Notodontidae, 267, 727 Papilionidae, 666, 685, 727 Pinus (tree), 730
Notonecta, 5, 26, 108, 179, 181, 335, 374, Papilionoidea, 190, 194, 665 Piophila, 168, 173
462–4, 621, 735 Parachartergus, 732 Platambus, 728
Notonectidae, 735 Parlatoria, 273 Plataspis, 321
Notostira, 331–2 Passalidae, 685 Plathemis, 674
Nycteribiidae, 86, 353–4 Passalus, 688 Platycleis, 682–3, 693
Nymphalidae, 381 Pectinophora, 112, 365, 661 Platygaster, 355, 372
Pediculus, 24, 89, 346, 501, 523 Platygasteridae, 371
Ocypus, 326 Pentatomidae, 45, 52, 707 Platymeris, 35, 52
Odonata, 6, 9, 48, 94, 96, 98, 108, 115, 149, Pentatomomorpha, 314, 326, 328, 684 Platypleura, 688
151, 176, 186, 189–90, 192–3, 195–9, Perga, 606, 730 Platypodinae, 57, 83, 85
204–5, 210, 214, 231, 237, 252, 259, 268, Perilampidae, 371 Platyuridae, 674
746 TAXONOMIC INDEX
Plea, 621 Reduvioidea, 684 Siphonoperla, 171, 192, 273, 278, 725
Plecoptera, 6, 43, 95, 98, 101, 115, 148–9, Requena, 288 Siricidae, 85
190, 204, 265–6, 277, 299, 303, 346, 367, Reticulitermes, 273, 711, 736 Sitophilus, 53–4, 65, 89, 492, 500
373, 393, 465, 480, 681, 696, 698 Rhagoletis, 84, 296, 648, 705, 718–19 Sminthurides, 11
Plodia, 53, 306, 705 Rhinocoris, 364 Smittia, 349
Plusia, 355, 371, 671 Rhinotermitidae, 273, 705, 725 Solenobia, 356–7
Podura, 174, 429, 431 Rhodnius, 23–4, 27–9, 30, 35, 40, 51, 54, 59, Solenopsis, 729, 730, 736
Poecilobothrus, 602 61–2, 104, 111, 120–1, 132, 156, 219, 243, Speophyes, 526
Poekilocerus, 729, 731, 733 249, 284–5, 289, 302, 306, 310, 313, 317, Sphaerius, 471
Polistes, 230, 234–5, 728, 734 326–30, 345, 367, 373, 377–8, 395, 415, Sphecoidea, 734–5
Polyctenidae, 352 422, 426–8, 447, 478, 482–6, 488–9, 491, Sphingidae, 267
Polydrosus, 392 494, 501, 547, 580, 604, 619, 663 Sphodromantis, 24
Polypedilum, 523 Rhogogaster, 555 Spodoptera, 58, 81, 90, 123, 245, 402–3, 503,
Polyphaga, 98, 299, 302 Rhopalosiphum, 521 592, 600, 641, 644, 649–50, 708–9,
Pompiloidea, 734 Rhyacophila, 380 711
Ponera, 587 Rhyacophilidae, 716 Staphylinidae, 157, 159, 371, 379, 591, 660,
Ponerinae, 686, 720, 722 Rhynchosciara, 59 728
Popillia, 205, 274, 276, 371 Rhyssa, 316 Staphylinoidea, 191
Potamodytes, 469–70 Riodinidae, 701 Stegobium, 88
Primicimex, 287 Romalea, 311, 499, 541, 673, 730 Stenobothrus, 686, 695
Prionoplus, 268, 274, 276 Rutilia, 234 Stenopelmatidae, 248
Prosopistoma, 266 Stenopsocus, 495
Protura, 8, 12, 31, 151–2, 259, 263, 273, 452, Sarcophaga, 18, 119–21, 135, 243–4, 252, Stenus, 175, 727
478, 587 351, 404, 406, 435, 458, 489, 521, 558 Stomoxys, 18, 42, 108, 290, 650
Psaltoda, 688, 695–6 Saturnia, 380, 391, 408 Streblidae, 353
Psammodes, 456–7 Saturniidae, 685 Strepsiptera, 159–60, 190, 192, 288, 351,
Psephenidae, 471 Satyridae, 666 355, 369–72, 382, 393, 478
Psephenoides, 471–2 Scarabaeidae, 47, 86, 447, 660, 666, 685, 716 Stylops, 355
Pseudaletia, 126, 244 Schistocerca, 8, 29, 31, 41, 45–8, 51, 73, 75, Supella, 79
Pseudococcus, 273 78–9, 84, 90, 106, 123, 126, 140, 155–6, Symmoracma, 689
Pseudosarcophaga, 70–1 159–60, 165, 167–70, 187, 195, 198, 201, Sympecma, 315
Psithyrus, 721 209, 211, 215–16, 230, 240, 248, 250–2, Sympetrum, 325, 393
Psocoptera, 34, 189–90, 194, 204, 231, 273, 269–70, 288, 296, 298, 312–13, 316, 344, Symphypleona, 263
300, 347, 351, 373, 495–7, 681 349–51, 356–7, 363, 365–6, 377, 379–80, Symphyta, 98, 189, 264, 314, 605
Psorophora, 290 423, 431, 434–5, 444–5, 450–2, 454–5, Synclysis, 710
Psychidae, 159, 356–7 459–61, 478, 480–3, 486–9, 491, 493, 500, Syrphidae, 209, 277, 587
Psychodidae, 273, 277 513–15, 527, 548–9, 555–6, 560–2, 574, Syrphus, 510
Psyllidae, 170, 197 576, 604, 614, 623, 630, 660, 662, 667–8,
Pteronidea, 108 690, 704, 723 Tabanidae, 278, 587
Pterophoridae, 191 Schizaphis, 266, 705 Tabanus, 220
Pteroptyx, 675–7 Schizophora, 277 Tachinidae, 351
Pterostichus, 405, 519 Sciara, 273–4, 347, 446, 523 Taeniochorista, 193
Ptinidae, 192 Sciaridae, 61 Taeniopoda, 97
Ptinus, 358, 523 Scolioidea, 734 Tanyptera, 371
Pulex, 547 Scolytidae, 715–16 Taphrophila, 470–2, 524
Pulicidae, 23 Scolytinae, 83, 713 Tekomyia, 359
Pyralidae, 689, 708 Scrophulariaceae (plants), 731 Telea, 10
Pyralidoidea, 621 Setaria (grass), 90 Teleogryllus, 238–40, 289, 313, 331, 431, 619,
Pyrgomorphidae, 288, 371 Sialis, 266, 284–5, 346, 482, 487, 500, 524 622, 631
Pyrops, 636 Simuliidae, 23, 381, 469, 471 Tenebrio, 43, 53–4, 58, 73, 77, 234, 237,
Pyrrhocoris, 406, 726 Simulium, 23, 107, 381, 387, 393, 464, 470, 269–70, 283, 340, 364, 385, 415, 478,
472 494–6, 500, 521, 573, 597, 606, 723
Ranatra, 684 Siphonaptera, 16, 23, 31, 82, 149, 299–300, Tenebrionidae, 591, 685, 707, 728
Reduviidae, 23, 52, 156 368, 373, 547, 587 Tenodera, 24–5, 321, 448, 590–1, 593
TAXONOMIC INDEX 747
larval development, 377 Lateral frontal organs, 576 mobilization 140, 211, 220, 306
metamorphosis, 367, 395–7 Learning, 82, 563–5 synthesis, 137–40
muscle degeneration, 242 Lecithin, 77 storage, 136, 137
oogenesis, 304 Lectin, 47, 122–3 transport, 53, 57, 112–14
lipid synthesis, 140 Leg, 151–60 water from, 498–9
pheromone synthesis, 713 blood supply, 98–101 yolk, 308
polyphenism, 400–1 development, 343, 382–5 Lipophorin, 112–4, 121, 134, 140, 303–4,
protein synthesis, 136 flight position, 211 308, 417, 578
vitellogenin synthesis, 304–7 functions, Lobula, 553, 556
influenced by, adhesion, 156 Locomotion, 160–81
parasitoids, 126 digging, 157–8 and see Flight, Leg
prothoracic gland, 578 grasping, 24–5, 157–8 Lubrication,
metabolism, 580 grooming, 158–9 mouthparts, 33
structure, 570–1 jumping, 169–73 silk tube, 34
synthesis control, 306, 572 landing, 214 Luciferase, 676
titer, 578–80 pollen collecting, 158 Luciferin, 676
transport, 113, 578 silk production, 159 Luminescence, 24, 674–7
sound production, 684–6 Lutein, 664
Katatrepsis, 340–1 swimming, 178–81 Lyonnet’s gland, 34
Kenyon cell, 551–4, 563 walking, 160–8 Lysozyme, 125–6, 390
Keratin, 55 muscles, 152–5, 167
Kin recognition, 723 reduction, 159–60 Macroplastron, 467–8
King termite, 723 sensilla, 155–6 Macropterous insects, 192
Kreb’s cycle, see Citric acid cycle tympanal organs, 622, 624–6 Macrotrichia, 190
Kynurenine, 661–2 Lens, see Compound eye, Ocellus, Stemma Magnesium, 501
Leptophragma, 496 dietary requirement, 78
Labellum, 17, 19–20 Lethal temperatures, 520–3 in hemolymph, 107–9, 115, 485, 487–90
Labial gland, 31–4, 392, 497 Leucopterin, 661, 669 light production, 676
Labial mask, 24–5 Leucokinin, 491, 543, 572 nerve conduction, 541
Labial palp, 13, 14, 16–19, 639 Levation, 162 utilization, 65
Labium, 12–16, 18–19, 24, 336, 341 Lift force, 209–10 Magnetic sensitivity, 600
Labrum, 12–13, 15–19, 336, 343 Lift/drag ratio, 168, 210 Magnetite, 600
Lacinate appendage, 272 Light, Makisterone, and see Ecdysteroid, 570–1
Lacinea, 13–14, 17 affecting color change, 670–2 Malpighian tubule, 478–80, 485–6, 489–90,
Lactic acid, 644 guide, 594, 596 519, 579
Lactic dehydrogenase, 241 limiting flight, cryptonephridial, 389, 494–6
Lamina, 553, 556, 595 production, 674–7 development, 345, 347, 376–7
Lancet, 314–15 sensitivity, and see Compound Eye, light production, 501
Landing, 214 Ocellus, Stemma metamorphosis, 388–9
Larva, brain, 607 nitrogenous excretion, 484–6
adult features in, 367–9, 382–6 dermal light, 606–7 numbers, 376, 378, 478
antenna, 9 transduction, 594–5 origin, 478
appendages, 382 Ligula, 14 salt regulation, 485–7, 489–90
cuticle, 367, 437 Lingual sclerite, 14 silk production, 501
development, 365–78, 382 Linoleic acid, 74–5 spittle production, 501
hatching, 363–6 Linolenic acid, 74–5 toxin excretion, 486
jumping, 173 Lipase, 35 water regulation, 489–96
locomotion, 173–6, 180–1 Lipid, Maltose, 55, 56, 73
pedogenesis, 358–9 absorption, 64 Mandible, 13–17, 20, 25
pheromones, 718–19, 724 cuticular, 406, 418–22, 435, 437, 492–3 adult emergence, 393
sound production, 685–6, 688, 701 dietary requirements, 70, 74–5 development, 343, 380
stemma, 605–6 digestion, 57 false, 392–3
types, 369–71 energy source 219–224 holding female, 278
Larviposition, 353 food reserve, 136–40 pheromone dispersal, 713–15
760 SUBJECT INDEX
eclosion hormone, 244, 394, 396–9, 572 Pharate condition, Pinene, 503
FMRFamide, 97, 542–3 368–70, 391, 393, 471 Piping, 691
growth blocking, 126 Pharyngeal pump, 23, 48, 50, 434 Pitching, in flight, 214, 216–17
hypertrehalosemic hormone, 570 Pharynx, 15, 38 in swimming, 179–80
ion transport peptide, 489, 491 Phenol, 69, 79, 114, 420, 432 Placoid sensillum, 636
leucokinin, 491, 543, 572 Phenoloxidase, 114, 121, 420, 433 Planta, 264
myotropic, 317 Phenylalanine, 55, 69–70, 72, 78–9, 111, Plasma, and see Hemolymph 107–16
affecting oviposition, 317 432–3, 487 Plasma membrane,
causing ovulation, 289 Pheromone, 558, 704–27 reticular system, 132–4, 417
pheromone biosynthesis peptide (PBAN), alarm, 266 Plasmatocyte, 116–25, 417
402, 543, 571–2, 577, 712 chemistry, 706–8 Plasticization of cuticle, 24, 397–9, 426–7
proctolin, 247–8, 270, 317, 542–5, 577 control of production, 712–15 Plastron, 329, 465–8, 470–2
prothoracicotropic hormone (PTTH), dispersal, 713–15, 718 Plate sensillum, 636
396–8, 543, 570–1, 577–8, 581–2 glands, 416, 704–7 Plectrum, 681
sex peptide, 289–90 production, 290–1, 416, 710–11 Pleural apophysis, 148–9
vasopressin-like hormone, 491 reception, 558, 641–5, 651 Pleural process, 148–9
Per gene, 565 regulating, Pleural ridge, 148
Percussion, 680–1 aggregation, 715–17 Pleural sulcus, 149, 153
Pericardial cell, see Nephrocyte alarm, 721–3 Pleuron, 148. 260–1
Pericardial sinus, 94–5 courtship, 717–18 Pleuropodium, 267, 343, 347, 352, 363
Perikaryon, 533 maturation, 723 Pleurostoma, 5
Perinephric sheath, 495–6 population density, 718–19 Pneumatization, 447–8
Perinephric space, 496 sexual behavior, 291, 715–21 Poikilotherm, 509
Perineural sinus, 94, 98 trail following, 719–21 Poison, see Venom
Perineurium, 535–6, 541 of social insects, 34, 723–5 Poison gland, 314, 706
development, 388 specificity, 708–10, 721 Polar body, 355
Periplasm, 333 synthesis, 710–11 Polar granule, 347
Peripneustic respiratory system, 448 Pheromone biosynthesis activating Polarized light, 600–1, 658
Peripodial cavity, 343, 383–5 neurohormone (PBAN), 402, 453, Pole,
Peripodial membrane, 120, 383–5 571–2, 577, 712–13 cell, 334, 336, 339, 347–8
Perispiracular gland, 461 Phloem feeding, 23, 61 plasm, 347
Peristigmatic gland, 416 Phosphate, 78, 115 Pollen,
Peritoneal sheath, 268, 270 Phosphatidyl choline, 77–8 basket, 158–9
Peritreme, 448 Phospholipid, 64, 78, 138–9 feeding 40, 53, 65
Peritrophic envelope, 44–7, 51, 57 Photocyte, 675–6 press, 158–9
Perivisceral fat body, 132, 135, 389 Photoperiod, 394, 396, 401–6, 565 Pollination, 701
Perivisceral organ, 577 Phragma, 145–6, 149, 197 Polydna virus, 126, 735
Perivisceral sinus, 94–5, 97–8 Physical, Polyembryony, 355–6
Permeability coefficient, 48 gill, 463 Polymorphism, see Polyphenism
Permeability constant, 452 color, 657–60 Polyneuronal innervation, 8, 197–9, 237–9
Petiole, 259 Phytecdysteroid, 74–7 Polyphenism, 355–6, 400–3
pH, Phytol, 503 color, 671
gut, 59 Pigment, Polyphenol, see Phenol
hemolymph, 116 color, 660–4 Polypneustic lobe, 354
Phagocytosis, epidermal, 416, 484 Polypneustic respiratory system, 448
of foreign bodies, 116, 122–3 eye screening, 135, 587–90, 592–3, 596–7, Polypod larva, 369, 371
in metamorphosis, 378, 386–7 599 Polysubstrate monooxygenase, 503–5
of sperm, 287 in hemolymph, 473 Polytene chromosomes, 132
Phagostimulant, 18–20, 29, 82, 651 movement, 665, 667, 669 Polytrophic ovariole, 300, 302
Phallic lobes, 277 of ocellus, 604 Pore canals, 418–19, 422–3, 493, 713
Phallobase, 277, 280 respiratory, 473–4 Porphyrin, 662–3
Phallomere, 277, 281 of retinula cell, 597–8 Postalar arm, 146, 149
Phallotreme, 277 of stemma, 606 Post-coxal bridge, 148–9
Phallus, and see Aedeagus, 269, 287 visual, 594–5, 599–600, 605 Post-embryonic development, 363–408
764 SUBJECT INDEX
Stance maintenance, 160 Subesophageal ganglion, 18, 20, 96, 248, Tarsomere, 151
Starch, digestion, 33, 55, 65, 73 546, 576 Tarsus, 151–2
Stearic acid, 74, 138–9 Substrate vibration, adhesion, 156–7
Steering, 211–12, 218 production, 681–2, 688, 691 articulation, 151–2
Stemma, 605–7 reception, 619–20 in locomotion, 178–81
Stenusin, 176 Suckers, modifications, 158–9
Sternal apophysis, 147–9 abdominal, 264, 278 musculature, 154
Sternellum, 146–9 tarsal, 157 pheromone, 724
Sternopleurite, 148 Sucrose, sensilla, 155–6
Sternum, 146, 148, 260 digestion, 33, 55 feeding, 20
Steroid, 570–1 feeding on, 24 flight, 210–11
in defense, 729 nutritional requirement, 73 Taste, see Chemoreception, Contact
Sterol, secretion, 736 chemoreceptor
absorption, 64 sensory perception, 82, 648–9 Tegmen, 191–2, 204, 682–5
in blood, 113 utilization, 73 Tegula, 194, 211
dietary requirements, 70, 74–7, 83, 570 Sugar, Telotrophic ovariole, 299, 301–2
from micro-organisms, 75, 83, 85, 88 storage, 51 Telson, 259, 337
in wax, 421 Sulcus, 3, 146, 423 Temperature, 509–16
Sting, and see Venom, 298, 314–15 Summation of synaptic inputs, 539–40 acclimation, 522–3
Stipes, 13–14, 20 Supercontraction, 244–5 affecting,
Stobbe’s gland, 705, 715 Supercooling, 518–21 activity, 515, 522
Stomatogastric nervous system, see Superlinguae, 15 color change, 513
Stomodeal nervous system Supination, of wing, 205–6 diapause, 404–7
Stomodeal nervous system, 33, 50–1, 236, Suspensory, embryonic development, 349–50,
344, 552 ligament, 295 365
Stomodeal valve, 40–1 sclerite, 4 emergence, 394
Stomodeum, see Foregut Suture, 3 enzyme activity, 59
development, 335–6, 339, 347 Swallowing, evaporative cooling, 516
Storage excretion, 483–4, 501 air, 393, 426, 431 flight, 250, 252, 510, 515
Strand receptor, 155, 631–2 extra-embryonic fluid, 363 hatching, 365
Streamlining, aquatic insects, 177 water, 431 heart rate, 104
Stretch receptor, 545, 629–33 Swimming, 176–81 metabolism, 515
and drinking, 495 speed, 180 morph of aphid, 401
feeding, 29–30, 427 Symbiont, see Micro-organism muscle action, 517
gut, 51 Synapse, 237, 245, 533–5, 539, 549 nervous output, 527–8
hormone release, 30 changes at, 597 oxygen consumption, 464
wing, 195–6, 211–12 electrical, 535, 539 physical gill efficiency, 464
Stridulation, 681–8 inhibitory, 549 pigmentation, 513
Strigil, 681 integration at, 549, 550, 560 sound production, 693, 695
Stroke plane, 202–3 numbers of, 535 survival, 518–22
Stylet, Synaptic, ventilation, 458
Apis sting, 315 cleft, 534, 539, 541, 544 walking speed, 165
sucking mouthpart, 15–16, 20–2 gap, 533 water loss, 492–3, 522
Stylus of Apterygota, 262–3 transmission, and see Neurotransmitter wingbeat frequency, 205, 515
Subalar sclerite, 148–9 vesicles, 238, 245, 534, 539, 544 of body, 509–17
Subcostal vein, 185–6 Synaptoid, 575 cold hardiness, 407
Subepidermal nerve plexus, 630 Systole, 95–6, 104 lethal, 520–3
Subgena, 5 preference, 514–15, 527
Subgenal sulcus, 4–5 Taenidia, 103, 441–2, 453 Q10, 205
Subgenital plate, 265, 277 Take-off, 210–11 receptor, 524–7
Subgenual organ, 156, 619–21 Tannic acid, 46 regulation, 515–17
Subimago, 393 Tanning, see Sclerotization sensitivity, 407, 524–5
Submentum, 13–14 Tapetum, 473, 589, 594 Tenent hairs, 156–7
Subesophageal body, 346 of ocellus, 604 Teneral period, 239
768 SUBJECT INDEX