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 ADVANCES IN INVERTEBRATE
(NEURO)ENDOCRINOLOGY
A Collection of Reviews in the Post-Genomic Era

VOLUME 2: Arthropoda
Taylor & Francis
Taylor & Francis Group
http://taylorandfrancis.com
 ADVANCES IN INVERTEBRATE
(NEURO)ENDOCRINOLOGY
A Collection of Reviews in the Post-Genomic Era

VOLUME 2: Arthropoda

Edited by
Saber Saleuddin, PhD
Angela B. Lange, PhD
Ian Orchard, DSc, PhD
Apple Academic Press Inc. Apple Academic Press Inc.
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Advances in Invertebrate (Neuro) Endocrinology, A Collection of Reviews in the Post-Genomic Era
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Library and Archives Canada Cataloguing in Publication

Title: Advances in invertebrate (neuro)endocrinology, two volumes : a collection of reviews in the post-genomic era /
edited by Saber Saleuddin, PhD, Angela Lange, PhD, Ian Orchard, DSc, PhD.
Names: Saleuddin, Saber, editor. | Lange, Angela, 1957- editor. | Orchard, Ian, 1951- editor.
Description: Includes bibliographical references and indexes. | Contents: Volume 2: Arthropoda.
Identifiers: Canadiana (print) 2019018860X | Canadiana (ebook) 20190188677 | ISBN 9781771888097 (set ; hardcover) |
ISBN 9781771888936 (v. 2 ; hardcover) | ISBN 9780429264450 (set ; ebook)
Subjects: LCSH: Invertebrates—Endocrinology. | LCSH: Neuroendocrinology.
Classification: LCC QP356.4 .A38 2020 | DDC 573.412—dc23

Library of Congress Cataloging-in-Publication Data

Names: Saleuddin, Saber, editor. | Lange, Angela, 1957- editor. | Orchard, Ian, 1951- editor.
Title: Advances in invertebrate (neuro)endocrinology : a collection of reviews in the post-genomic era / edited by
Saber Saleuddin, Angela Lange, Ian Orchard.
Description: Oakville, ON ; Palm Bay, Florida : Apple Academic Press, [2020] | Includes bibliographical references and index.
| Contents: v. 1. Phyla other than Arthropoda -- v. 2. Arthropoda. | Summary: “Advances in Invertebrate (Neuro)Endocrinology:
A Collection of Reviews in the Post-Genomic Era (2-volume set) provides an informative series of reviews from expert
scientists who are at the forefront of their research into the endocrinology of invertebrates. These two volumes are timely
and appropriate in this post-genomic era because of the rapid pace of change brought about by genome projects, functional
genomics, and genetics (omics technologies). The volumes show the rich history and strong tradition of cutting-edge research
using invertebrates that has opened up our broader understanding of comparative endocrinology and the evolution of regulatory
pathways and systems. These reviews set the scene and context for this exciting new era of understanding that has come
from this post-genomic revolution. This book undertakes the daunting task of covering most of the diverse endocrine systems
that exist among invertebrates. The papers in this book will advance our knowledge of invertebrate endocrinology but also of
endocrinology in general, making the book valuable to researchers and students. Key features: Looks at the enormous diversity
of species involved and the variety of hormonal pathways covers the diverse endocrine systems that exist among invertebrates
makes relevant comparisons of molecular, cellular, and behavioral aspects of invertebrate endocrinology Explores the
molecular genetics techniques are now allowing exploitation of these genomes through specific interference with genes, and
thereby interference with their phenotypic expression”-- Provided by publisher.
Identifiers: LCCN 2019042135 | ISBN 9781771888097 (set ; hardcover) | ISBN 9781771888929 (v. 1 ; hardcover) |
ISBN 9781771888936 (v. 2 ; hardcover) | ISBN 9780429264450 (ebook)
Subjects: MESH: Neurosecretory Systems--physiology | Invertebrates--physiology | Invertebrates--genetics |
Hormones--physiology | Neuropeptides--physiology | Neuroendocrinology
Classification: LCC QP356.4 | NLM WL 102 | DDC 612.8--dc23
LC record available at https://lccn.loc.gov/2019042135
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electronic format. For information about Apple Academic Press products, visit our website at www.appleacademicpress.com and the CRC Press
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 DEDICATION
“Knowledge advances progress, whereas ignorance impedes it.”
This book is dedicated to Dr. Berta Scharrer for her pioneering
work in (neuro)endocrinology and to our parents for giving us the
encouragements and opportunities to become biologists.
Taylor & Francis
Taylor & Francis Group
http://taylorandfrancis.com
About the Editors

Saber Saleuddin, PhD

Saber Saleuddin, PhD, is a University Professor Emeritus in the Department
of Biology, York University in Toronto, Ontario, Canada. He received his
early education in Bangladesh and his doctorate from the University of
Reading in the UK. His studies on biomineralization in mollusks started
at the University of Alberta in Edmonton, Canada, and continued at Duke
University, Durham, North Carolina, in the laboratory of Karl Wilbur. Though
offered a teaching position at Duke University, he accepted a faculty position
at York University, where he still teaches. His outstanding contributions in
teaching, research, and administration were recognized by York University.
He has published extensively in international journals and has co-edited five
books on molluscan physiology. He served as co-editor of the Canadian
Journal of Zoology for 18 years and was president of the Canadian Society of
Zoologists, from whom he received a Distinguished Service Medal.

Angela B. Lange, PhD

Angela B. Lange, PhD, is a world leader in the field of insect neuroendocri-
nology, with over 175 research publications and numerous invited research
talks at international and national conferences. Professor Lange also demon-
strates leadership in the research community, being a Council Member of
the North American Society of Comparative Endocrinology, the European
Society of Comparative Endocrinologists, and the International Federation
of Comparative Endocrinology Societies. In addition to her international
stature in research, Professor Lange was Chair of the Department of Biology,
Acting Vice-Principal and Dean, and is currently Vice-Dean, Faculty, at the
University of Toronto Mississauga, Ontario, Canada. She obtained her BSc
and PhD degrees from York University, Canada.

Ian Orchard, DSc, PhD

Ian Orchard, DSc, PhD, is a Professor Emeritus, Biology, of the University of
Toronto, Ontario, Canada. An expert in insect neuroendocrinology with over
200 research publications, Professor Orchard has been funded by the Natural
Sciences and Engineering Council of Canada since 1980, has chaired the
viii About the Editors

NSERC Animal Physiology Grant Selection Committee, and has presented

numerous invited keynote and plenary research talks at international
conferences. Professor Orchard served as a Vice President of the University
of Toronto and Principal of the University of Toronto Mississauga (2002–
2010) and Vice President Academic and Provost, University of Waterloo
(2014–2017), Canada. He earned a BSc (1972), PhD (1975), and DSc
(1988), all from the University of Birmingham, UK.
Contents

Contributors ..................................................................................................... xi
Abbreviations.................................................................................................. xiii
Preface ............................................................................................................ xix

1. Juvenile Hormone Regulation and Action .................................................... 1

C. Rivera-Pérez, M. E. Clifton, F. G. Noriega, and M. Jindra

2. Molecular Functions of Ecdysteroids in Insects.......................................... 77

Naoki Yamanaka and Naoki Okamoto

3. Adipokinetic Hormone: A Hormone for All Seasons? ............................. 129

Heather G. Marco and Gerd Gäde

4. Sex-Related Peptides of Male Insects ........................................................ 177

R. E. Isaac and S. Sturm

5. Endocrine Control of Pupal Diapause in the

Cabbage Army Moth Mamestra brassicae................................................. 195
Akira Mizoguchi

6. Hormonal Control of Diuresis in Insects .................................................. 225

Ian Orchard and Angela B. Lange

7. Stayin’ Alive: Endocrinological Stress Responses in Insects .................. 283

Atsushi Miyashita and Shelley A. Adamo

8. Insect GPCRs and Development of Mimetic Analogs of the

Insect Kinin, Pyrokinin-Like, and Sulfakinin Neuropeptide
Classes as Pest Management Tools ............................................................ 325
R. J. Nachman

Index .................................................................................................................... 375

Taylor & Francis
Taylor & Francis Group
http://taylorandfrancis.com
Contributors

Shelley A. Adamo
Department of Psychology and Neuroscience, Dalhousie University, Halifax, NS, B3H4R2, Canada

M. E. Clifton
Collier Mosquito Control District, Naples, FL, USA

Gerd Gäde
Department of Biological Sciences, University of Cape Town, Private Bag,
ZA-7701 Rondebosch, South Africa.
R. E. Isaac
School of Biology, University of Leeds, Leeds LS2 9JT, UK

M. Jindra
Biology Center, Czech Academy of Sciences, Institute of Entomology, Ceske Budejovice,
Czech Republic, E-mail: jindra@entu.cas.cz

Angela B. Lange
Department of Biology, University of Toronto Mississauga, Mississauga, Ontario, Canada

Heather G. Marco
Department of Biological Scienc, University of Cape Town, Private Bag,
ZA-7701 Rondebosch, South Africa

Atsushi Miyashita
Department of Psychology and Neuroscience, Dalhousie University, Halifax, NS, B3H4R2, Canada

Akira Mizoguchi
Professor of Biology, Division of Liberal Arts and Sciences, Aichi Gakuin University, Nisshin, Aichi,
470-0195, Japan, Tel.: +81-561-73-1111, Fax: +81-561-73-1860, E-mail: amizo@dpc.agu.ac.jp

R. J. Nachman
Insect Control and Cotton Disease Research Unit, Southern Plains Agricultural Research Center,
ARS, U.S. Department of Agriculture, 2881 F-B Road, College Station, TX 77845, USA

F. G. Noriega
Department of Biological Sciences and Biomolecular Science Institute, Florida International University,
Miami, FL, USA, E-mail: noriegaf@fiu.edu

Naoki Okamoto
Department of Entomology, University of California, Riverside, Riverside CA 92521, USA

Ian Orchard
Department of Biology, University of Toronto Mississauga, Mississauga, Ontario, Canada

C. Rivera-Pérez
CONACyT-Centro de Investigaciones Biológicas del Noroeste (CIBNOR), La Paz, B.C.S.,
México (Northwest Biological Research Center (CIBNOR), La Paz, B.C.S., México.)

S. Sturm
School of Biology, University of Leeds, Leeds LS2 9JT, UK
xii Contributors

Naoki Yamanaka
Department of Entomology, University of California, Riverside, Riverside CA 92521, USA
Abbreviations

AC adenylate cyclase
ACE angiotensin converting enzyme
ACP adipokinetic-corazonin-related peptide
ADFs antidiuretic factors
ADFα antidiuretic factor α
ADFβ antidiuretic factor β
AG accessory glands
AKH adipokinetic hormone
AKHR AKH receptor
AMP antimicrobial peptide
AMPK AMP-activated protein kinase
AST allatostatins
AT allatotropin
AVP arginine-vasopressin peptide
BBC backbone cyclic
BMS Bombyx myosuppressin
BRFa Bombyx FMRFamide-related peptide
CA corpora allata
cAMP cyclic adenosine monophosphate
CAP2b cardioacceleratory peptide 2b
CAP2b cardioactive peptide 2B
CBP CREB-binding protein
CC corpus cardiacum
CC-CA complex corpora cardiaca-corpora allata complex
CCK cholecystokinin
CHC cuticular hydrocarbons
CHH crustacean hyperglycemic hormone
CHO Chinese hamster ovary
CIC citrate carrier
CNS central nervous system
CRF corticotropin releasing-factor
CRF/DH corticotropin-releasing factor-related diuretic hormone
CT/DH calcitonin-related diuretic hormone
CTSH chloride transport stimulating hormone
xiv Abbreviations

DA dopamine
DD diapause-destined
DH diapause hormone
DMAPP dimethylallyl pyrophosphate
DMSO dimethylsulfoxide
DOPA dihydroxyphenylalanine
DPC dodecyl phosphocholine
DUM dorsal unpaired median
DUP99B ductus ejaculatorius peptide 99B
ELC2 extracellular loop 2
ELISA enzyme-linked immunosorbent assay
ER endoplasmic reticulum
ET early trypsin
ETH ecdysis triggering hormone
ETHR ETH receptor
FA farnesoic acid
FOL FPP to farnesol
FPP farnesyl pyrophosphate
FPPS FPP synthase
GAMs generalized additive models
GBP growth blocking peptide
GC-MS gas chromatography combined with mass spectrometry
GPA glycoproteins α
GPB glycoproteins β
GPCRs G-protein coupled receptors
GPP geranyl diphosphate
GSCs germline stem cells
HAD haloalkanoic acid dehalogenase
HDLp high-density lipophorin
HEK human embryonic kidney
HIF2α hypoxia-inducible factor 2α
HMGR HMG-CoA reductase
HMGS HMG-CoA synthase
HNF4 hepatocyte nuclear factor 4
HP-1 head peptide-1
HPLC high-performance liquid chromatography
IIS insulin/insulin-like signaling
IK insect kinin
ILPs insulin-like peptides
IP3 trisphosphate
Abbreviations xv

IPCs ILP-producing cells

IPP isopentenyl diphosphate
IPPI IPP isomerase
ITP ion transport peptide
ITPL ion transport peptide-like
JH juvenile hormone
JHA JH acid
JHAMT JH acid methyltransferase
JHB3 bis-epoxide JH III
JHBP JH binding proteins
JHD JH diol
JHDK juvenile hormone diol kinase
JHDP JH diol phosphate
JHE juvenile hormone esterase
JHEH juvenile hormone epoxide hydrolase
JHREs JH response elements
JHSB3 JH III skipped bisepoxide
KATP ATP-dependent potassium
LDLp l ow-density lipophorin
LE larval ecdysis
LGR1 leucine-rich repeat-containing GPCR1
LNSCs lateral neurosecretory cells
LPK leucopyrokinin
MAGs male accessory glands
MALDI matrix-assisted laser desorption ionization
MF methyl farnesoate
MIH molt-inhibiting hormone
MIP-1 myoinhibiting peptide-1
MIPs myoinhibitory peptides
MOIH mandibular organ inhibiting hormone
MPD 2-methyl-2,4-pentanediol
MRCH melanization and reddish coloration hormone
MTGM mesothoracic ganglionic mass
MTs myotropins
MVAP mevalonate pathway
NCC-RN nervi corporis cardiaci-recurrens
ND non-diapause-destined
NEP neprilysin
NES nuclear export
NKCC Na+/K+/Cl–/Cl–
xvi Abbreviations

NLS nuclear localization

NMA normal mode analysis
NMR nuclear magnetic resonance
NO nitric oxide
NPLP1 neuropeptide-like precursor 1
NPLP1-VQQ neuropeptide-like precursor1-VQQ
NPYLR1 neuropeptide Y-like receptor
NR nuclear receptor
NS-II cells neurosecretory-II cells
NUDT3 nucleoside diphosphate-linked moiety X motif 3
OA octopamine
OBP odorant-binding proteins
ODE ordinary differential equations
OMP ovary maturating parsin
PAMPs pathogen-associated molecular patterns
PAS Per-Arnt-Sim
PBAN pheromone biosynthesis activating neuropeptides
PCA principal component analysis
PCD programmed cell death
PDE phosphodiesterases
PE pupal ecdysis
PEG polyethylene glycol
PGs prothoracic glands
PI3K phosphatidylinositol-3-kinase
PK pyrokinin
PKA protein kinase A
PKB protein kinase B
PKC protein kinase C
PKG cGMP-dependent protein kinase
PLC phospholipase C
PMRs post-mating responses
PRO prothoracic ganglion
PSOs perisympathetic organs
PT pheromonotropin
PTSP prothoracicostatic peptide
PTTH prothoracicotropic hormone
PVKs periviscerokinins
RAMPs receptor activity modifying proteins
RCP receptor component protein
RMSF root-mean-square fluctuation
Abbreviations xvii

RNAi RNA interference

ROS reactive oxygen species
RPCH red pigment-concentrating hormone
RRS1 regulator of ribosome synthesis 1
RT-FIA time-resolved fluoroimmunoassay
SAM S-adenosyl-L-methionine
SAR structure-activity relationship
SF seminal fluid
SKR SK receptors
SKs sulfakinins
SOG subesophageal ganglion
SP sex peptide
SPR SP receptor
TAGs triacylglycerols
TALEN transcription activator-like effector nuclease
TEP transepithelial potential
TGF-β transforming growth factor-beta
TH tyrosine hydroxylase
THIOL the enzymes acetoacetyl-CoA thiolase
TM transmembrane
TMOF trypsin modulating oostatic factor
TOF-MS time-of-flight mass spectrometry
TOR target of rapamycin
TR-FIA time-resolved fluoroimmunoassay
TRPs tachykinin-related peptides
TULIP tubular lipid-binding proteins
UCP4 uncoupling protein 4 gene
UCPs uncoupling proteins
USP Ultraspiracle
VIH vitellogenesis-inhibiting hormone
VMNSCs ventral midline neurosecretory cells
Preface

Neuroendocrine control of cellular activities first evolved in invertebrates,

and the presence of endocrine cells was first reported in a mollusk. Both
peptidergic and lipid-derived hormones have been found in invertebrates,
and a few hormones are unique to invertebrates. Berta Scharrer, along with
her husband, Ernst, were the first to coin the term “neuroendocrinology.”
Later, Berta, based on her work on Aplysia (mollusks) and Nereis (an annelid)
in the early 1930s, introduced the term “neurosecretion.” As a result of her
subsequent work on arthropods, the concept (neuroendocrinology/neurose-
cretion) became accepted by the scientific community.
This series of reviews bring together expert scientists who are at the
forefront of their research into the endocrinology of invertebrates. These
two volumes are timely and appropriate in this so-called post-genomic era.
Timely, because of the pace of change brought about by genome projects,
functional genomics, and genetics (‘omics technologies), including tran-
scriptomics, peptidomics, proteomics, metabolomics, gene microarrays, and
sophisticated mass spectrometry techniques. Appropriate, because of the rich
history and strong tradition of cutting edge research using invertebrates that
have opened up our broader understanding of comparative endocrinology
and the evolution of regulatory pathways and systems. These reviews set
the scene and context for this exciting new era we find ourselves in, and the
depth of understanding that has come from this post-genomic revolution.
Studies broadly defined as invertebrate endocrinology have been
transformed over the last two decades since the original sequencing of the
Drosophila genome. Sequenced genomes are now available for many inver-
tebrates, and a bold initiative is underway to sequence genomes from 5,000
arthropod species (the i5k project; http://i5k.github.io/). This project, along
with other invertebrate projects, is transformative and is consolidating the
discipline in this 21st century. These projects have global implications, since
invertebrates are so important in; for example, agriculture (pollination, crop
destruction), aquaculture and other food sources, medicine (toxins, analge-
sics), and industry (silk). Researchers are now able to approach questions
concerned with evolution and phylogeny, and make relevant comparisons
of molecular, cellular, and behavioral aspects of invertebrate endocrinology.
These comparisons can be made between invertebrates, but also between
xx Preface

invertebrates and vertebrates, since another bold initiative, the Genome 10K
project, aims to assemble the genomes of 10,000 vertebrate species (https://
genome10k.soe.ucsc.edu/).
Developments in molecular genetics techniques are now allowing
exploitation of these genomes through specific interference with genes, and
thereby interference with their phenotypic expression. Functional genomics
and genetics are, therefore, helping to unravel complex regulatory processes.
The genes and proteins at all levels of the endocrine signaling pathway are
being defined. Gene and peptide expression can be determined for specific
tissues and individual cells, and experimental manipulation in their expres-
sion can aid in an understanding of endocrine regulation and physiology.
Editing a review series on invertebrate endocrinology is a difficult task
because of the enormous diversity of species involved and the variety of
hormonal pathways. Though we are aware it is a daunting task, this book
covers the diverse endocrine systems that exist among invertebrates. In
spite of our sincere desire, we were unable to find contributions in certain
groups because of the unavailability of contributors. Thus, the list of papers
in this book is based on expert colleagues willing and able to write within the
allotted time frame. In order to compensate for the absence of certain topics/
fields, we have reproduced two already published papers.
We are indeed indebted to those colleagues who contributed to this
book and gratefully acknowledged the role of reviewers who, with their
thoughtful comments, made our work easier. We hope that the papers in this
book will advance our knowledge of invertebrate endocrinology but also of
endocrinology in general and that the book will be valuable to researchers
and students.
Finally, we are grateful to Sandra Jones Sickels and Ashish Kumar of
Apple Academic Press for their support in every step involving planning,
editing, printing, and marketing.
CHAPTER 1

Juvenile Hormone Regulation and Action

C. RIVERA-PÉREZ,1 M. E. CLIFTON,2 F. G. NORIEGA,3 and M. JINDRA4
1
CONACyT-Centro de Investigaciones Biológicas del Noroeste (CIBNOR)
[Northwest Biological Research Center (CIBNOR)], La Paz, B.C.S., México.
2
Collier Mosquito Control District, Naples, FL, USA
3
Department of Biological Sciences and Biomolecular Science Institute,
Florida International University, Miami, FL, USA, E-mail: noriegaf@fiu.edu
4
Biology Center, Czech Academy of Sciences, Institute of Entomology,
Ceske Budejovice, Czech Republic, E-mail: jindra@entu.cas.cz

1.1 INTRODUCTION

Sesquiterpenoid hormone production in bilaterians shares a conserved

mevalonate biosynthetic pathway, which originates from acetate and dates
back to a common ancestor in the Ordovician (approximately 444–488
mya). The pathway diverged to generate various final products in different
taxa, namely cholesterol in vertebrates, juvenile hormone (JH) in insects,
and methyl farnesoate (MF) and farnesoic acid (FA) in crustaceans (Kenny
et al., 2013; Cheong et al., 2015). The JHs are a family of insect acyclic
sesquiterpenoids produced by the corpora allata (CA), a pair of endocrine
glands connected to the brain (Tobe and Stay, 1985; Goodman and Cusson,
2012; Hiruma and Kaneko, 2013). The JHs are involved in the regulation
of reproduction, metamorphosis, behavior, caste determination, diapause,
stress response, and numerous polyphenisms (Nijhout, 1994; Riddiford,
1994; Wyatt and Davey, 1996; Hartfelder and Emlen, 2012; Jindra et al.,
2013; Zhu and Noriega, 2016; Roy et al., 2018; Santos et al., 2019). It is
likely that early in the evolution of insects, the original function of JH was
to regulate adult female reproduction before it was co-opted as a hormone
controlling metamorphosis (Tobe and Bendena, 1999).
2 Advances in Invertebrate (Neuro)Endocrinology, Volume 2

The field of JH research thrives in the post-genomic era. In the last years,
seminal progress has been made in our understanding of the regulation
of JH titers and mode of action. We can highlight the identification of all
the enzymes involved in JH synthesis, and the measurement of changes in
transcripts, JH precursor metabolites, and enzymatic activities in the minute
CA of insects (Nouzova et al., 2011; Rivera-Perez et al., 2014). The elusive
intracellular JH receptor has been discovered (Charles et al., 2011; Jindra et
al., 2013) and its mode of binding to JH and to JH-response DNA elements
has been partially unveiled (Charles et al., 2011; Li et al., 2011, 2014; Kayu-
kawa et al., 2012; Bittova et al., 2019). A JH signaling pathway that regu-
lates metamorphosis has been supported with genetic evidence from diverse
insect models (Konopova and Jindra, 2007, 2008; Minakuchi et al., 2009;
Riddiford et al., 2010; Konopova et al., 2011; Ureña et al., 2014; Bellés
and Santos, 2014; Jindra et al., 2015b; Daimon et al., 2015; Kayukawa et
al., 2017). The repertoire of target genes downstream of the JH receptor
has been explored (Zou et al., 2013; Saha et al., 2016). A new branch of
plasma membrane-initiated JH signaling has been put forward (Liu et al.,
2015). This chapter aims to provide an overview of general aspects on JH
biosynthesis, transport, and degradation, as well as mechanisms of action
and roles of JH in controlling development and reproduction in insects.

1.2 REGULATION OF JH TITERS

JH titers are regulated by the balance between biosynthesis and release of

the hormone from the CA, as well as its degradation and clearance from the
hemolymph by tissue uptake and excretion (Feyereisen, 1985; Goodman and
Cusson, 2012). Numerous studies indicate that JH biosynthesis is a major
regulator of JH titer; it is also widely accepted that JH is not stored in the
CA and therefore the amount of JH released to the incubation medium or
hemolymph represents the amount of JH synthesized (Feyereisen, 1985;
Hernandez-Martinez et al., 2015).

1.2.1 JH SYNTHESIS

1.2.1.1 JH HOMOLOGUES

Eight different forms of JH have been identified, and at least one JH homolog
has been detected in more than 100 insect species (Goodman and Cusson,
Juvenile Hormone Regulation and Action 3

2012) (Figure 1.1). It is estimated that more than 2.5 million insect species
inhabit the earth (Mora et al., 2011); therefore, it is conceivable that addi-
tional forms of JH could be discovered in the future. The first JH (JH I)
was identified in the moth Hyalophora cecropia (Röller et al., 1967), and
its structure was later established as a 2E, 6E, 10-cis isomer (Dahm et al.,
1968), with a chiral center 10R, 11S (Meyer et al., 1971). Four additional
JHs have been reported in Lepidoptera: JH 0, JH II, JH III and 4-methyl JH
I (Meyer et al., 1968, 1971; Judy et al., 1973; Bergot et al., 1981) (Figure
1.1). JH III is the homolog found in the majority of insects (Goodman and
Cusson, 2012; Rivera-Perez et al., 2014). The CA of Drosophila melano-
gaster and other brachyceran Diptera secrete a bis-epoxide JH III (JHB3)
(Richard et al., 1989), as well as MF (Harshman et al., 2010; Wen et al.,
2015) (Figure 1.1). The possible role of MF as a “JH” in insect preimaginal
stages was a controversial issue that is just starting to be addressed (Wen et
al., 2015; Jindra et al., 2015b). MF is abundant in the hemolymph of imma-
ture stages of several insects (Teal et al., 2014), including 4th instar larvae
of Aedes aegypti mosquitoes (Hernandez-Martinez et al., 2015). MF is the
immediate biosynthetic precursor of JH in mosquitoes, and therefore is very
abundant in CA extracts (Rivera-Perez et al., 2014). On the other hand, MF
is not released by the CA of adult A. aegypti, and it is undetectable in the
hemolymph of adult females (Hernandez-Martinez et al., 2015). Another
bis-epoxide form, JH III skipped bisepoxide (JHSB3) is present in some
heteropterans such as Plautia stali (Kotaki et al., 2009, 2011) (Figure 1.1).
All these JH homologs share common structural features which might
be necessary for a full biological activity; they contain a methyl ester (α,
β-unsaturated) moiety group at the C1 position and an epoxide group at the
C10-C11 position. JHB3 and JHSB3 have an additional epoxide group at
C2-C3 and C6-C7, respectively. Hydroxylated JHs are generally considered
products of the biological inactivation of JHs (Goodman and Cusson, 2012);
though, in some insect species, they have been described as more active than
the non-hydroxylated forms (Darrouzet et al., 1997).
JH has long been considered a target for the development of novel insec-
ticides (Williams, 1967; Slama et al., 1974; Cusson et al., 2013). Different
approaches have been used to identify natural products and to create synthetic
compounds with anti-JH activities, such as inhibition of JH biosynthesis, increase
in JH catabolism or interference of JH signaling. In addition, juvenoids, such
as methoprene, are functional mimics of the endogenous JHs and true agonists
of the intracellular JH receptor (Jindra et al., 2015b; Jindra and Bittova, 2019)
that can prevent metamorphosis (Jindra et al., 2013) or interfere with normal
reproduction (Staal, 1986; Cusson et al., 2013).
4 Advances in Invertebrate (Neuro)Endocrinology, Volume 2

FIGURE 1.1 JH homologs.

Chemical structures of juvenile hormone homologs isolated from insects.
Juvenile Hormone Regulation and Action 5

1.2.1.2 CORPORA ALLATA (CA) AND OTHER SYNTHETIC TISSUES

The principal endocrine organ responsible for JH synthesis is the CA, a pair
of endocrine glands connected to the brain (Tobe and Stay, 1985; Hiruma and
Kaneko, 2013). In larvae of higher Diptera the CA are in close association
with another neuroendocrine organ, the corpora cardiaca (CC), and along
with a third endocrine gland, the prothoracic gland (PG), are fused into the
ring gland or “gland complex” (Burgess and Rempel, 1966). The size, shape,
and composition of the gland complex changes as a fly or mosquito pupae
transform into adults (Burgess and Rempel, 1966). The most important of
these changes is the PG degeneration, a programmed cell death process
(Martau and Rommer, 1998).
Innervation of the CA plays a key role in the regulation of CA activity
(Tobe and Stay, 1985; Goodman and Cusson, 2012). In mosquitoes, stimula-
tory and inhibitory effects of brain factors have been described (Li et al.,
2004; Hernandez-Martinez et al., 2007); separation of the CA from the brain
(denervation) results in a remarkable activation of JH synthesis in early pupae
(Areiza et al., 2015). In contrast, denervation prevents the 10-fold activation
of JH synthesis that occurs 12 h after adult eclosion (Hernandez-Martinez et
al., 2007). In sugar-fed and blood-fed females, denervation causes a signifi-
cant increase in JH synthesis (Li et al., 2004). All these results indicate that
stimulatory and inhibitory brain factors control CA activity.
It has been suggested that JH could be produced in organs other than the
CA. Some insect males transfer JH, present in the accessory glands (AG),
to females at mating (Shirk et al., 1980; Clifton et al., 2014), but there is no
clear evidence if JH is synthesized de novo in the AG, or just sequestered
there from the hemolymph. The AG of H. cecropia moths contains a JH
acid (JHA) methyltransferase (JHAMT) that methylates JHA in the pres-
ence of S-adenosyl-L-methionine (SAM) (Peter et al., 1981). It has been
recently suggested that the adult gut populations of intestinal stem cells and
enteroblasts, are a new source of JHs in D. melanogaster (Rahman et al.,
2017). This local and gut-specific JH activity is synthesized by and acts on
the intestinal stem cell and enteroblast populations, regulating their survival
and cellular growth through the JH receptor Gce and its partner Tai (see
Section 1.3). Recently a lepidopteran betaentomopoxvirus has been reported
to encode a JHAMT. The recombinant protein has a SAM-dependent
methyltransferase activity (Takatsuka et al., 2017). The gene is expressed in
virus-infected insect tissues, and the protein accumulates in the hemolymph.
There, it transforms JHA into JH, thus inhibiting host metamorphosis. This
6 Advances in Invertebrate (Neuro)Endocrinology, Volume 2

inhibition is advantageous for viral transmission in host insect popula-

tions via increased virus production and inhibition of pupation-associated
behavior.

1.2.1.3 JH SYNTHESIS PATHWAY

The biosynthetic pathway of JH in the CA of insects includes 13 enzymatic

reactions, and it is generally divided into early and late steps (Nouzova et
al., 2011; Goodman and Cusson, 2012) (Figure 1.2). The early steps follow
the mevalonate pathway (MVAP) to form farnesyl pyrophosphate (FPP)
(Belléset al., 2005). First, three units of acetyl-CoA are condensed into meval-
onate through three sequential steps involving the enzymes acetoacetyl-CoA
thiolase (THIOL), HMG-CoA synthase (HMGS) and HMG-CoA reduc-
tase (HMGR) (Figure 1.2). Mevalonate is later converted to isopentenyl
diphosphate (IPP) via three enzymatic reactions catalyzed by mevalonate
kinase (MevK), phosphomevalonate kinase (P-MevK), and mevalonate
diphosphate decarboxylase (PP-MevD), respectively (Nouzova et al.,
2011). FPP synthase (FPPS), a short-chain prenyltransferase, generates FPP
by completing two sequential couplings: first IPP and dimethylallyl pyro-
phosphate (DMAPP) condense in a head-to-tail manner to produce geranyl
diphosphate (GPP). This type of head-to-tail condensation is repeated by the
further reaction of GPP with IPP yielding FPP (Figure 1.2).
Insect FPP syntheses (FPPS) are typically active as homodimers (Bellés
et al., 2005; Sen et al., 1996; 2006; 2007a; 2007b). In the mustard leaf beetle
Phaedon cochleariae (Frick et al., 2013) and A. aegypti (Rivera-Perez et
al., 2015), FPPSs possess an interesting product regulation mechanism; they
change the chain length of their products depending on the cofactor present.
The protein produces C10-GPP in the presence of Co2+ or Mn2+, while it
yields the longer C15-FPP in the presence of Mg2+. That allows insects to
supply precursors for different terpene pathways using a single enzyme.
The production of DMAPP, the allylic isomer of IPP, is catalyzed by an
IPP isomerase (IPPI). Insect IPPIs requires Mg2+ or Mn2+ for full catalytic
activity (Diaz et al., 2012).
The enzymes of the MVAP are well conserved in eukaryotes. In insects,
all the MVAP enzymes seem to be encoded by single-copy genes, and iden-
tification of predicted amino acid sequences was possible based on sequence
homology (Noriega et al., 2006; Kinjoh et al., 2007; Nouzova et al., 2011).
Nevertheless, biochemical characterization of purified or recombinant
enzymes of the MVAP in insects is limited to HMGS (Sen et al., 2012),
Juvenile Hormone Regulation and Action 7

HMGR (Martinez-Gonzalez, 1993; Buesa et al; 1994), MevK (Nyati et al.,

2015) IPPI (Diaz et al., 2012) and FPPS (Bellés et al., 2005; Sen et al., 1996;
2006; 2007a; 2007b; Cusson et al., 2006; Rivera-Perez et al., 2015).

FIGURE 1.2 JH biosynthesis pathway.

Precursors are connected by arrows. Enzymes are shown in italics. Abbreviations for the
enzymes are between the parenthesis. Cofactors are in smaller letters and connected to the
pathway by arrows.
8 Advances in Invertebrate (Neuro)Endocrinology, Volume 2

In the late steps comprising the JH-specific branch (Figure 1.2), conver-
sion of FPP to farnesol (FOL) is catalyzed in D. melanogaster by a FPP
phosphatase (FPPase or FPPP) (Cao et al., 2009), a member of the NagD
haloalkanoic acid dehalogenase family (HAD), with orthologues in several
insect species, including A. aegypti (Nyati et al., 2013). The mosquito
FPPase (AaFPPase-1) is an Mg2+ dependent NagD HAD protein that effi-
ciently hydrolyzes FPP and GPP, but not IPP (Nyati et al., 2013). Subse-
quently, FOL undergoes two sequential oxidation reactions that generate
farnesol and FA (Figure 1.2). In mosquitoes, the first reaction is catalyzed
by a short chain farnesol dehydrogenase (AaSDR-1), a member of the “clas-
sical” NADP-dependent cP2 SDR subfamily that presents broad substrate
and tissue specificity (Mayoral et al., 2009b). Oxidation of FOL into FAL
in mosquitoes is effected by an NAD+-dependent aldehyde dehydrogenase
class 3 (AaALDH3-1) showing tissue and developmental-stage-specific
splice variants (Rivera-Perez et al., 2013). Homologs of farnesol and farnesol
dehydrogenases having similar activities in the CA of other insects have not
yet been described.
The order of the last two biosynthetic steps, methyl esterification and
epoxidation (Figure 1.2), catalyzed by a JHAMT (Shinoda and Itoyama,
2003) and a P450 monooxygenase epoxidase (EPOX) (Helvig et al.,
2004), differs among insects (Defelipe et al., 2011; Goodman and Cusson,
2012). In the Lepidoptera, epoxidation precedes esterification by JHAMT
(Shinoda and Itoyama, 2003). In the Orthoptera, Dictyoptera, Coleoptera,
and Diptera, epoxidation follows methylation (Defelipe et al., 2011). In all
insect species studied, recombinant JHAMTs were able to methylate JHA
and FA at similar rates (Shinoda and Itoyama, 2003; Minakuchi et al., 2008a;
Niwa et al., 2008; Sheng et al., 2008; Mayoral et al., 2009a; Marchal et al.,
2011). Homology modeling and docking simulations confirmed that JHAMT
is a promiscuous enzyme capable to methylate FA and JHA (Defelipe et
al., 2011). In contrast, epoxidases have narrow substrate specificity; while
the EPOX from the cockroach Diploptera punctata efficiently epoxidizes
MF and is unable to process FA (Helvig et al., 2004), Bombyx mori EPOX
exhibits at least 18-fold higher activity for FA than for MF (Daimon et al.,
2012). Therefore, the order of the methylation and epoxidation reactions
may be primarily imposed by the epoxidase’s substrate specificity (Defelipe
et al., 2011). In the Lepidoptera, epoxidase has higher affinity than JHAMT
for FA, so epoxidation precedes methylation, while in most other insects
there is no epoxidation of FA, but esterification of FA to form MF, followed
by epoxidation to JH III.
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Bergen-op-Zoom in 1814, when lying wounded there, after the
unfortunate failure of that well-planned attack.’

RUMINANTIA.
The ruminants furnish, as is well known, the largest portion of our
animal food, being consumed by man alike in civilized or unsettled
countries. The domestic animals require little notice at our hands.
There are, however, some whose flesh is eaten in different countries
that are less familiar. Thus the bison and musk-ox of North America,
the reindeer of Greenland and Northern Europe—the various
antelopes, the gnu, the giraffe, and the camel of Africa, and the
alpaca tribe of South America, supply much of the animal food of the
people in the districts where they are common.
The flesh of the camel is dry and hard, but not unpalatable.
Heliogabalus had camels’ flesh and camels’ feet served up at his
banquets. In Barbary, the tongues are salted and smoked for
exportation to Italy and other countries, and they form a very good
dish. The flesh is little esteemed by the Tartars, but they use the
hump cut into slices, which, dissolved in tea, serves the purpose of
butter.
The flesh of the Axis deer (Cervus axis, or Axis maculata) is not
much esteemed in Ceylon, having little fat upon it, and being very
dry. The India samver, or musk deer, is eaten there.
The flesh of the great moose deer or elk, of North America, the
carcase of which weighs 1,000 or 1,200 lbs., is as valuable for food
as beef, but from its immense size, much of the flesh is usually left in
the forest.
It is more relished by the Indians and persons resident in the fur
countries, than that of any other animal, and bears a greater
resemblance in its flavour to beef than to venison. It is said that the
external fat is soft like that of a breast of mutton, and when put into a
bladder is as fine as marrow.
The flesh of the caribboo, a smaller animal, rarely exceeding 400
lbs., is less palatable than moose venison. Nor is the flesh of the red
or Virginian deer much better, although the venison dried is very
good.
Venison is not ‘meat’ in the parlance of the backwoodsman; that
term, as Sam Slick tells us, is reserved par excellence for pork; and
he is frequently too indolent or too much occupied otherwise, to hunt,
although deer tracks may be seen in every direction around the
scene of his daily rail-splitting operations. He considers it cheaper to
buy venison of the Indians, when there are any Indians in the locality.
But venison has some solid value even in those parts, and if salted
and smoked, would be entitled to a place among the articles of
household thrift.
Of the Arctic quadrupeds, the reindeer (Cervus tarandus) is most
valuable, its flesh being juicy, nutritious, and well-flavoured, and easy
of digestion. They abound in Greenland, and are tolerably numerous
in Melville Island.
In Sweden, roast reindeer steaks and game are dressed in a manner
preferable to that which prevails with us. The flesh is first perforated,
and little bits of lard inserted; and, after being baked in an oven, it is
served in a quantity of white sauce.
The flesh of the young giraffe is said to be good eating. The
Hottentots hunt the animal principally on account of its marrow,
which, as a delicacy, they set a high value on.
The Hottentots have a curious mode of cooking their antelope
venison, which renders it, however, exceedingly palatable. After
stewing the meat in a very small quantity of water, they take it out of
the pot and pound it between two stones until reduced to the
consistency of pap, when they mix it with a considerable quantity of
sheep’s fat, and then stew it for a short time longer. This is an
excellent way of preparing dry flesh of any kind.
‘On one occasion’ (says Lieut. Moodie), ‘after I had taken out my
share of this mess, the Hottentots added a larger quantity of fat to it
to please their own palates; and one of them ate so heartily of the
greasy mixture, that he became seriously unwell, but recovered by
chewing dry roots of the sweet-scented flag (Calamus aromaticus).
This plant is very much used by the Dutch for stomach complaints,
and they generally cultivate some of it in wet places in their gardens.’
The eland of Africa (Boselaphus Oreas) is the largest of the antelope
tribe, its size being indicated by its generic name. The bulls attain to
the height of nineteen hands at the shoulder, and frequently exceed
1,000 lbs. in weight. It fattens readily on the most meagre herbage of
the desert, and to the delicious, tender, juicy, and wholesome nature
of its flesh every hunter will bear witness, who has regaled himself
on the steaks broiled in the homely style of South African cookery,
with some of the usual condiments or spices to give them an
unnatural relish. The flesh has a peculiar sweetness, and is tender
and fit for use the moment the animal is killed.
It is hunted with avidity, on account of the delicacy of its flesh, but is
very rarely found within the limits of the Cape Colony, having been
driven beyond the Orange River by the progress of colonization.
The hartebeest, an antelope of the size of the Scotch red deer,
though now rather rare, is much prized by the African sportsman. It is
also called caama by the Dutch farmers, and is a favourite object of
pursuit with both natives and colonists. The flesh is rather dry, but of
a fine grain, more nearly resembling the beef of the ox than that of
any other antelope, except, perhaps, the so-called eland or elk of the
colonists (A. oreas, Pallas), and it has a high game flavour which
makes it universally esteemed.
The meat of the sassaby (A. lunata, Burchell), a rare species, is
tender and well tasted. The flesh of the ourebi of Southern Africa (A.
scoparia, Schreber), though dry and destitute of fat, is esteemed one
of the best venisons of the country.
The flesh of the bosh-bok, or bush goat, as its colonial name implies
(A. sylvatica, Sparrman), makes good venison, that of the breast
being particularly esteemed. The flesh of the rheebok (A. capreolus,
Lichstenstein) is dry and insipid, and relished less than that of any
other of the numerous Cape antelopes. The bush antelope (A.
silvicultrix, Afzelius) affords excellent venison, and is much sought
after on that account. The flesh of the ahu (A. subgutturosa,
Guldenstaedt) is excellent, and of an agreeable taste. That of the
gnu of South Africa is in great repute both among the natives and
Dutch settlers. Though the meat has a wildish flavour, it is more juicy
than that of most of the antelope tribe, and very much like beef.
The flesh of the alpaca and guanaco is sold in the public shambles
of Peru, Chili, &c.
Sheep’s milk is a common beverage in Toorkistan, where the sheep
are milked regularly three times a day. Goats are very scarce; cows
not to be seen; but the sheep’s milk affords nourishment in various
forms, of which the most common is a kind of sour cheese, being
little better than curdled milk and salt.
If we think ox tails a delicacy, Australians (as we have seen) like
kangaroo tails, and the Cape colonists have fat sheep’s tails
requiring a barrow or a cart on which to support them. The broad fat
tail, which often composes one-third of the weight of the animal, is
entirely composed of a substance betwixt marrow and fat, which
serves very often for culinary purposes instead of butter; and being
cut into small pieces, makes an ingredient in various dishes.
The dried flesh of the argali, or wild sheep, is in Kamtschatka an
article of commerce.
The domestic goat’s flesh is not in much favour anywhere, although
that of a young kid, three or four months old, is very tender and
delicate. Some of the goats are eaten in the Cape Colony, but the
flesh is generally lean and tough. The Malabar goat is a delicate
animal, that browzes on the rocks. It is more sought after than any
game in Ceylon, for, contrary to the general nature of the goat, its
flesh is tender and excellent when broiled.
Bison beef, especially that of the female, is rather coarser grained
than that of the domestic ox, but is considered by hunters and
travellers as superior in tenderness and flavour. The hump, which is
highly celebrated for its richness and delicacy, is said, when properly
cooked, to resemble marrow. The flesh of the buffalo, as it is
misnamed, is the principal, sometimes the only, food of numerous
tribes of North American Indians. It is eaten fresh on the prairies
during the hunt, and dried in their winter villages.
The musk-ox (Ovibos moschatus) is of much importance from its
size and palatable rich meat. It has occasionally furnished a rich
meal to arctic explorers. When they are fat, the flesh is well
flavoured, but smells strongly of musk.

CETACEA.
The flesh of the manatus is white and delicate, and tastes like young
pork eaten fresh or salted, while the fat forms excellent lard. The
cured flesh keeps long without corruption, and it will continue good
several weeks, even in the hot climate of which it is a native, when
other meat would not resist putrefaction for as many days. The fibres
and the lean part of the flesh are like beef, but more red; it takes a
very long time boiling. The fat of the young one is like pork, and can
scarcely be distinguished from it, while the lean eats like veal. The
fat, which lies between the entrails and skin has a pleasant smell,
and tastes like the oil of sweet almonds. It makes an admirable
substitute for butter, and does not turn rancid in the sun. The fat of
the tail is of a firmer consistence, and when boiled is more delicate
than the other.
Manatees, or sea calves, are found in certain parts of British
Honduras in great numbers. They are, according to my friend, Chief
Justice Temple, frequently caught and brought to the market of
Belize, where they are snapped up with the greatest avidity. He
states the flesh to be white and delicate, something between pork
and veal. The tail, which is very fat, is most esteemed. This caudal
luxury is generally soused or pickled. I do not, myself, fancy the flesh
of this brute, for it is so inhumanly human—it reminds one so much
of a mermaid, or of one of the fifty daughters of Nereus, that to eat it
seems to me to be an approximation to cannibalism. It appears
horrible to chew and swallow the flesh of an animal which holds its
young (it has never more than one at a litter) to its breast, which is
formed exactly like that of a woman, with paws resembling human
hands. But these notions would be considered highly fantastic by
those who masticate a monkey with the greatest relish, partake with
gusto of rattlesnake soup, and voraciously devour an alligator stew.
The manatus is commonly found in shallow water, at the mouths of
rivers, where it feeds upon the marine herbage which there grows in
great luxuriance. It has no teeth, but two thick, smooth, hard,
unserrated bones run from one side of the mouth to the other. I am
inclined to think that these bones might be used as a substitute for
ivory.[11]
Mr. P. H. Gosse, in his interesting little manual on the Natural History
of the Mammalia, remarks:—
‘From personal experience we can confirm Hernandez’s statement of
the excellence of the flesh of the manatee; he truly compares it to
well fatted pork, of pleasant flavour. The pursuit of it, on this account,
has rendered it scarce in many localities, where it was formerly
numerous; in the vicinity of Cayenne, it was at one time so common,
that a large boat might be filled with them in a day, and the flesh was
sold at 3d. per pound. About the middle of the last century it fetched,
at Port Royal in Jamaica, 15d. currency per pound.’
The tongue of the sea-lion (Phoca jubata) is very good eating, and
some seamen prefer it to that of an ox or calf. Thus Dr. Pernetty
(Voyage to the Falkland Islands) says,—‘For a trial we cut off the tip
of the tongue hanging out of the mouth of one of these lions which
was just killed. About sixteen or eighteen of us ate each a pretty
large piece, and we all thought it so good that we regretted we could
not eat more of it.
‘It is said that their flesh is not absolutely disagreeable. I have not
tasted it, but the oil which is extracted from their grease is of great
use. This oil is extracted in two ways; either by cutting the fat in
pieces and melting it in large caldrons upon the fire, or by cutting it in
the same manner upon hurdles or pieces of board, and exposing
them to the sun, or only to the air. This grease dissolves of itself and
runs into vessels placed underneath to receive it. Some of our
seamen pretended that this last sort of oil, when it is fresh, is very
good for kitchen uses. It is preferred to that of the whale; is always
clear, and leaves no sediment.’
Walrus meat is strong, coarse, and of a game-like flavour. Seal flesh
is exceedingly oily, and not very palatable; but by practice, residents
in the northern regions learn to relish both exceedingly.
The large tongue, the heart, and liver of the walrus (Trichecus
rosmarus), are often eaten by whalers for want of better fresh
provisions, and are passably good.
Commodore Anson’s party killed many sea-lions for food, using,
particularly, the hearts and tongues, which they thought excellent
eating, and preferable even to those of bullocks. The flesh of the
female sea-bear (Phoca ursina, Lin.) they found very delicate, having
the taste of lamb; while that of the cub could scarcely be
distinguished from roasted pig.
Sir Edward Parry was once asked, at a dinner where Lord Erskine
was present, what he and his crew had lived upon when they were
frozen in in the Polar Seas. Parry said they lived upon seals. ‘A very
good living, too,’ exclaimed the Chancellor, ‘if you keep them long
enough.’
One of the ordinary acts of hospitality and civility on the part of the
Esquimaux ladies, is to take a bird, or piece of seal-flesh, chew it up
very nicely, and hand it to the visitor, who is expected to be
overcome with gratitude, and finish the operation of chewing and
digesting the delicate morsel.
The carcase and blubber of the whale at Bahia, in Brazil, are
reduced to food by the poor.
To most of the rude littoral tribes of Northern Asia and America, the
whale and seal furnish, not only food and clothing, but many other
useful materials. The Esquimaux will eat the raw flesh of the whale
with the same apparent relish, when newly killed, or after it has been
buried in the ground for several months.
The whales on the coasts of Japan not only afford oil in great
abundance, but their flesh, which is there considered very
wholesome and nutritious, is largely consumed. No part of them,
indeed, is thrown away; all is made available to some useful purpose
or another. The skin, which is generally black, the flesh, which is red
and looks like coarse beef, the intestines and all the inward parts,
besides the fat or blubber, which is boiled into oil, and the bone,
which is converted into innumerable uses,—all is made available to
purposes of profit.
Both sperm and black whales abound on the coast of Western
Australia. Sometimes a dead whale is thrown on the shore, and
affords luxurious living to the natives. They do not, however, eat the
shark.
The natives of New Zealand, when short of food, will not scruple to
eat the flesh of the whale, when caught in their vicinity.
The deep has many food dainties as well as the land, as we shall
shortly have to notice, and among these is the porpoise, which the
reader may probably have seen dashing up our rivers, or, during a
long voyage, disporting itself amid the briny waves, and rolling
gracefully near the sides of the ship. This sea pig sometimes serves
for a feast. When caught, it is cut into steaks, dried, and put into the
ship’s coppers, with a quantum suf. of spices and condiments which
nearly overpower the oily taste. The steaks turn blackish on being
exposed to the air, but this is ‘a matter of nothing’ to those whose
daily diet is usually limited to hard biscuits and salt junk. Landsmen
may question the niceness of the palate which partakes of this
dainty, but the old adage holds true everywhere, ‘de gustibus non
disputandum.’ There is no disputing about tastes.
According to ancient records, salted porpoises were formerly used
for food in this country.
In the olden times, when glass windows were considered an
effeminate luxury, and rushes supplied the place of carpets, the flesh
of the porpoise constituted one of the standard delicacies of a public
feast. It was occasionally served up at the tables of the old English
nobility as a sumptuous article of food, and eaten with a sauce
composed of sugar, vinegar, and crumbs of fine bread. But tastes
have altered, and even sailors will scarcely touch the flesh now. M.
de Bouganville, in his voyage to the Falkland Islands, writes—‘We
had some of the porpoise served up at dinner the day it was taken,
which several others at the table besides myself thought by no
means so ill-tasted as it is generally said to be.’
Porpoises are rather dangerous enemies to the shoals of fish. A
porpoise, before taking in a barrel of herrings for its dinner, will often
whet its appetite with a cod’s head and shoulders, leaving the tail
part for some poor fisherman.
 BIRDS.
Leaving now our passing survey of the food supplies derived from
animals, we come next to birds, and, in the first order, we do not find
that any are eaten, at least, as far as my knowledge extends; indeed,
these carnivorous birds, from their habits and their food, would not
be very tempting. This, however, as we have seen in the case of
predatory animals, is no safe criterion to judge from. Probably, the
man who would feast on the flesh of a lion, or a polecat, would have
a stomach strong enough to digest slices of a John Crow carrion
vulture, an eagle, or a hawk.
In the order of Insessores, or perching birds, I may mention first—
The becafico, or fig-eater (Sylvia hortensis), a bird about the size of
a linnet, which is highly prized by the Italians for the delicacy of its
flesh, particularly in autumn, when it is in excellent condition for the
table.
There is a curious food product obtained, (not exactly, however, from
the bird,) which is in high repute in China; and that is the edible nest
of a species of swallow extensively obtained in some of the islands
of the Eastern Archipelago.
These nests are attached to the sides of rocks like those of our
martin and swallow to walls, and look like so many watch-pockets.
The eggs are white, with a slight pinkish tinge, and are generally two
in number. The nests are either white, red, or black, and the natives
maintain that these are built by three distinct species, with a white,
red, and black breast, but this is erroneous. The Malays assert
frequently, moreover, that the nests are formed from the bodies of
certain sea snakes, but the food is, without doubt, insects. The
subjoined accounts furnish the most detailed information known
respecting the collection and trade in these birdsnests.
The following description of the birdsnests’ rocks, in the district of
Karang Bollong, on the southerly sea-coast of Java, is given in the
first volume of the Journal of the Indian Archipelago, published at
Singapore.
‘The gathering of these nests takes place three times a year—in the
end of April, the middle of August, and in December. The yearly
produce is commonly between 50 and 60 piculs of 133⅓ lbs. The
business of collection is opened with great ceremony by the natives.
By the assistance of ladders and stages made of rattan, the
collectors descend the rocks and cliffs, provided with the requisite
bags to contain the nests, which are taken from the wall by the hand,
and those which are on the roof by an iron hook made fast to a long
bamboo. The birds feed upon different kinds of bloodless insects,
hovering above the stagnant waters, for which their wide open beak
is very useful. They form their nests by vomiting the strongest and
best fragments of the food which they have eaten. The nests are
weighed and packed in hampers (of 25 catties each), and labelled
with the net weight, mark of the overseer, &c., and then further
preserved and secured with strips of bark, leaves, and matting.
‘The edible birdsnests, which owe their celebrity only to the
whimsical luxury of the Chinese, are brought principally from Java
and Sumatra, though they are found on most of the rocky islets of
the Indian Archipelago. The nest is the habitation of a small swallow,
named (from the circumstance of having an edible house) Hirundo
esculenta. They are composed of a mucilaginous substance, but as
yet they have never been analyzed with sufficient accuracy to show
the constituents. Externally, they resemble ill-concocted, fibrous
isinglass, and are of a white colour, inclining to red. Their thickness
is little more than that of a silver spoon, and the weight from a
quarter to half an ounce. When dry they are brittle and wrinkled; the
size is nearly that of a goose’s egg. Those that are dry, white, and
clean, are the most valuable. They are packed in bundles, with split
rattans run through them to preserve the shape. Those procured
after the young are fledged, are not saleable in China. The quality of
the nest varies according to the situation and extent of the caves,
and the time at which they are taken. If procured before the young
are fledged, the nests are of the best kind; if they contain eggs only,
they are still valuable; but if the young are in the nests, or have left
them, the whole are then nearly worthless, being dark-coloured,
streaked with blood, and intermixed with feathers and dirt. These
nests are procurable twice every year; the best are found in deep,
damp caves, which, if not injured, will continue to produce
indefinitely. It was once thought that the caves near the sea-coast
were the most productive; but some of the most profitable yet found
are situated 50 miles in the interior. This fact seems to be against the
opinion that the nests are composed of the spawn of fish, or of
bêche-de-mer. The method of procuring these nests is not
unattended with danger. Some of the caves are so precipitous, that
no one but those accustomed to the employment from their youth
can obtain the nests, being only approachable by a perpendicular
descent of many hundred feet, by ladders of bamboo and rattan,
over a sea rolling violently against the rocks. When the mouth of the
cave is attained, the perilous task of taking the nests must often be
performed by torchlight, by penetrating into recesses of the rock;
where the slightest slip would be instantly fatal to the adventurers,
who see nothing below them but the turbulent surf, making its way
into the chasms of the rock—such is the price paid to gratify luxury.
After the nests are obtained, they are separated from feathers and
dirt, are carefully dried and packed, and are then fit for the market.
The Chinese, who are the only people that purchase them for their
own use, bring them in junks to this market, where they command
extravagant prices; the best, or white kind, often being worth four
thousand dollars per picul (a Chinese weight, equal to 133⅓ lbs.
avoirdupois), which is nearly twice their weight in silver. The middling
kind is worth from twelve to eighteen hundred, and the worst, or
those procured after fledging, one hundred and fifty to two hundred
dollars per picul. The majority of the best kind are sent to Pekin, for
the use of the court. It appears, therefore, that this curious dish is
only an article of expensive luxury amongst the Chinese; the
Japanese do not use it at all, and how the former people acquired
the habit of indulging in it, is only less singular than their persevering
in it. They consider the edible birdsnest as a great stimulant, tonic,
and aphrodisiac, but its best quality, perhaps, is its being perfectly
harmless. The labour bestowed to render it fit for the table is
enormous; every feather, stick, or impurity of any kind is carefully
removed; and then, after undergoing many washings and
preparations, it is made into a soft, delicious jelly. The sale of
birdsnests is a monopoly with all the governments in whose
dominions they are found. About two hundred and fifty thousand
piculs, of the value of one million four hundred thousand dollars, are
annually brought to Canton. These come from the islands of Java,
Sumatra, Macassar, and those of the Sooloo group. Java alone
sends about thirty thousand pounds, mostly of the first quality,
estimated at seventy thousand dollars.’[12]
Mr. J. H. Moor, in his notices of the Indian Archipelago, published at
Singapore some years ago, states, that ‘one of the principal and
most valuable articles of exportation is the edible birdsnests, white
and black. These are found in much greater abundance in and about
the Coti, more than any other part of Borneo, or from what we at
present know on the subject, all parts put together. On the western
coast they are scarcely known to exist; about Banjermassin and
Bagottan there are none; at Bataliching and Passier they are found
in considerable quantities. At Browe there is abundance of the black
kind of a very superior quality, but little of the white. At Seboo, and all
the parts to the north of Borneo, we know there is none, as I have
seen many letters from different Rajahs of those countries averring
the fact, and begging the Sultan of Coti to exchange his edible nests
for their most valuable commodities, and at his own price. Nor ought
this to create surprise, when we consider, not only the large
consumption of this article by the Cambojans, who almost
exclusively inhabit some of the largest Sooloo Islands, and the
northern parts of Borneo, but the amazing demand on the whole
coast of Cambodia, particularly of Cochin China, the principal
inhabitants of which countries are as partial to this luxury as their
more northern neighbours—the Chinese. There are in Coti and
adjacent Dyak countries perhaps eighty known places, or what the
natives term holes, which produce the white nests. I have seen the
names of forty-three. There can, however, be no doubt there are
many more likewise known to the Dyaks, who keep the knowledge to
themselves, lest the Bugis should dispossess them, which they know
from experience is invariably the case.
‘According to the accounts of the Sultan, rendered by Saib Abdulla,
the bandarree in 1834 yielded 134 piculs. The usual price in money
to the Coti traders is 23 reals per catty from the Dyaks, and 25 in
barter. The black nests may be procured in great abundance. The
best kinds come from Cinculeram and Baley Papang. The latter
mountain alone yields 230 piculs (of 113⅓ lbs.). Cinculeram gives
nearly as much. There are several other parts of Coti which produce
them, besides the quantity brought down by the Dyaks. Last year,
130 piculs paid duty to the Sultan; these left the large Coti river.
Those from Cinculeram and Bongan were taken to Browe and
Seboo. The bandarree’s book averages the annual weight of those
collected in the lower part of Coti at 820 piculs (about 1,025 cwts.)
‘The Pangeran Sierpa and the Sultan say they could collect 2,700
piculs of black nests, if the bandarree and capella-campong would
behave honestly. The Sultan, however, seldom gets any account of
what is sent to Browe, Seboo, and the Sooloo Islands, the quality of
which is far superior to any sent to European ports.’
The exports of birdsnests from Java, between 1823 and 1832,
averaged about 250 piculs a year; in 1832, 322 piculs; but of late
years the exports have not averaged half that amount; and in 1853
and 1854 there were only about 35 or 40 piculs shipped.
In the third order, Scansores, there are very few edible birds.
In the mountain of Tumeriquiri, in the government of Cumana, is the
immense cavern of Guacharo, famous among the Indians. It serves
as a habitation for millions of nocturnal birds (Steatornis caripensis, a
new species of the Caprimulgis, of Linnæus), whose fat yields the oil
of Guacharo.
Once a year, near midsummer, this cavern is entered by the Indians.
Armed with poles, they ransack the greater part of the nests, while
the old birds hover over the heads of the robbers as if to defend their
brood, uttering horrible cries. The young which fall down are opened
on the spot. The peritoneum is found loaded with fat, and a layer of
the same substance reaches from the abdomen to the vent, forming
a kind of cushion between the hind legs. Humboldt remarks that this
quantity of fat in frugivorous animals, not exposed to the light, and
exerting but little muscular motion, brings to mind what has been
long observed in the fattening of geese and oxen. ‘It is well known,’
he adds, ‘how favourable darkness and repose are to this process.’
At the period above mentioned, which is generally known at Carissa
by the designation of ‘the oil harvest,’ huts are built by the Indians,
with palm leaves, near the entrance and even in the very porch of
the cavern. There the fat of the young birds just killed is melted in
clay pots, over a brushwood fire, and this fat is named butter or oil of
the Guacharo. It is half liquid, transparent, inodorous, and so pure
that it will keep above a year without turning rancid.[13]
There is a curious bird met with in caves in the West India Islands—
as at Dominica, and the gulf of Paria, the diablotin or goat-sucker,
which, if eaten when taken from the nest, is pronounced by epicures
unrivalled; and the flesh is also considered a delicacy when salted.
It has received its popular cognomen from its ugliness, but I have not
been able to trace its scientific name.
The bird is nearly the size of a duck, and web-footed, with a big
round head and crooked bill like a hawk, and large full eyes like an
owl; the head, part of the neck, and chief feathers of the wing and
tail, are black, while the other parts of its body are covered with a
fine milk-white down; the whole appearance being very singular. The
diablotin only leaves its haunts at night time, flying with hideous
screams like the owl, which it resembles in its dislike to day-light.
The nests are made in holes in the mountains. When the palms are
in fruit, the bird becomes one lump of fat. The hideous appearance
of the bird and the strong scent once got over, it is said to be a
delicious morsel.
We have our delicate tit-bits in spitted larks, and as many as four
thousand dozen have been known to be taken in the neighbourhood
of Dunstable between September and February. What the number
sold in our metropolitan markets is annually, it is impossible to say.
But larks are taken in much larger numbers in Germany, where there
is an excise upon them, which has yielded as much as £1,000 a year
in Leipsic—the larks of which place are famous all over Germany as
being of a most delicate flavour.
In the Italian markets, besides carrion crows, strings of thrushes,
larks, and even robin redbreasts are sold.
Young rooks, when skinned and made into pies are much esteemed
by some persons, but they are very coarse eating.
One of the most delicious birds is the rice-bunting of South Carolina
(Dolichonyx oryzivorus).
The rice-bunting migrates over the continent of America, from
Labrador to Mexico, and over the great Antilles, appearing in the
southern extremity of the United States about the end of March.
Towards the middle and close of August, they enter New York, and
Pennsylvania on their way to the south. There, along the shores of
the large rivers lined with floating fields of wild rice, they find
abundant subsistence, grow fat, and their flesh becomes little inferior
in flavour to that of the European ortolan, on which account the reed,
or rice birds, as they are then called, are shot in great numbers.
When the cool nights in October commence, they move still farther
south, till they reach the islands of Jamaica and Cuba in prodigious
numbers to feed on the seeds of the guinea grass. Epicures
compare the plump and juicy flesh of this delicacy to the ortolan.
On the shores of the Mediterranean there are feathered delicacies in
the shape of the quail and the ortolan. Thousands of ortolans used to
be shipped from the island of Cyprus, packed in casks of 300 or 400,
prepared with spice and vinegar. When specially fattened for the
table, they are regarded as most delicious; but, being merely lumps
of fat, are so rich as soon to satiate the appetite of even a professed
gourmand. In the West India Islands and the Southern States of
America, the rice-bunting, as we have seen, takes its place, and is,
occasionally, found in prodigious numbers, and greatly esteemed.
The bluish flesh of the toucan, notwithstanding its enormous and
unsightly beak, is a wholesome and delicate meat; and there are no
birds that give the Trinidad epicure a more delicious morsel. It is one
of the most omnivorous of birds, and its powers of digestion and
impunity to poisons are remarkable.
Parrot pie is said to be pretty good; at least, it may be so when other
animal food is scarce.
Among the gallinaceous fowls, large numbers contribute to the
food delicacies of man. Some, like the turkey, peacock, &c., of
considerable size; others, as the pigeon tribe, form smaller tit-bits.
The game birds, the pheasant, partridge, grouse, &c., and the quail,
guinea fowl, and jungle fowl, are bagged whenever they can be
obtained by the sportsman.
The peacock enkakyll ‘was one of the famous dishes at the costly
royal banquets of old, and the receipt for dressing it is thus given:—
‘Take and flay off the skin with the feathers, tail, and the neck and
head thereon; then take the skin and all the feathers and lay it on the
table abroad, and strew thereon ground cumin; then take the
peacock and roast him, and baste him with raw yolks of eggs; and
when he is roasted, take him off and let him cool awhile, then take
him and sew him in his skin, and gild his comb, and so serve him
forth with the last course.’
As far as my own experience goes, with all the basting and sauces,
the peacock is, at best, a dry and tough eating bird.
The domestic fowls and the tame turkey require no notice here, there
being nothing curious about them, however delicate eating they may
be when properly fattened and brought to table; but there is a
species of wild turkey found in New Granada, weighing from 12 to 16
lbs., and called the iowanen, which is described by Mr. W. Purdie of
Trinidad as the most delicate article of food he ever tasted.
Dear as fowls, ducks, and eggs comparatively are, they meet, as
every one knows, with a ready sale. When we find our imports of
eggs, chiefly from France, amount to about 130,000,000 a year,
besides our nominal ‘new laid,’ or home produce,—when we learn
that the foreign poultry we receive (mixed up with not a few Ostend
rabbits) is valued at 39,000l., and that Ireland supplies us with about
150,000,000 of eggs, we begin to perceive that fowls, ducks, geese,
and turkeys must be a profitable investment to some persons, and
the capital of about 4,000,000l. we lay out on these various products
serves to gladden the heart of many a poultry breeder.
There are sent to market about nine or ten million head of poultry in
a year to supply the whole population of the United Kingdom,
shipping and all, which is not more than one-third of a fowl to each
person annually. Now, were every one to have a fowl as part food
once a month, it would require 330,000,000 more fowls or other
poultry than are at present sold.
I copy the following from what I believe to be the first fixed tariff of
provisions, in the City of London, about the second year of Edward I.
(1272.) The people had at that time great cause to complain of the
exorbitant prices demanded of them for provisions, by hucksters and
dealers, and a fixed price was found necessary by the Mayor:—
The best hen three half-pence
Pullet three half-pence
Capon two pence
Goose five pence
Wild goose four pence
Pigeons, three for one penny
Mallard, three for a half-penny
Plover one penny
Partridge three half-pence
Larks, per dozen one penny half-penny
Pheasant four pence
Heron six pence
Swan three shillings
Crane three shillings, and by
a subsequent Act one shilling
The best peacock one penny
The best coney, with skin four pence
Ditto, without skin three pence
 The best hare, with skin three pence half-penny
The best lamb, from
Christmas to Lent six pence
At other times of the year four pence.
In the time of Edward II., 1313, eggs were 20 a penny, and pigeons
sold at three for a penny.
It is curious, even to notice the London prices of poultry, two or three
centuries ago, although regard must of course be had to the
difference in the value of money now and then.
Sir James Hawes, during his mayoralty, in the year 1575, fixed the
following prices within the City of London:—
s. d.
Blackbirds, per dozen 0 10
The best capon, large and fat 1 8
Ditto, second best, being fat 1 4
The best green goose, until Whitsuntide 0 8
Ditto ditto, after Whitsuntide 0 10
Ditto, in winter, being fat 1 2
Pigeons, per dozen 1 4
Chickens, the largest, each 0 4
Ditto, second sort 0 3
The best coney rabbit, from and after the
summer 0 5
Eggs, four 0 1
Cygnets, fat until Allhalloweentide, each 6 0
Ditto, from then to Shrovetide 7 0
Cranes, the best, each 6 0
The best heron, pheasant, shoveller (duck),
and bittern, each 2 6
Turkey-cock, fat and large 3 0
Turkey chicken, fat and large 1 4
Woodcocks, each 0 6
 Snipes, each 0 2½
Hens, being fat and the best, each 0 9
Ditto, second sort 0 7
Green plovers, fat 0 4
The best wild mallard 0 6
Teals, each 0 3
At a feast given at Ely House, by the serjeants-at-law, November,
1531, (23rd of Henry VIII.) on the occasion of making eleven new
serjeants, open house was kept for five successive days. On the
fourth day, King Henry, his Queen, the Foreign Ambassadors, the
Judges, and Lord Mayor and Aldermen, were feasted, as also
numerous guests, knights, and gentlemen. Stow particularizes the
following articles and prices, in order to furnish data for computing
the relative value of money at different periods:—
s. d.
Great beeves, from the shambles
(twenty-four) each 26 8
One carcase of an ox 24 0
Fat muttons (one hundred), each 2 10
Great veals (fifty-one), each 4 8
Porks (thirty-four), each 3 8
Pigs (ninety-one), each 0 6
Capons of Greece (of one poulterer, for they
had three) ten dozen, each capon 1 8
Capons of Kent (nine dozen and six), each 1 0
Capons, coarse (nineteen dozen), each 1 0
Cocks of grouse (seven dozen and nine), each
cock 0 8
Cocks, coarse (fourteen dozen and eight) 0 3
Pullets, the best, each 0 2½
Other pullets, each 0 2
Pigeons (thirty-seven dozen), at per dozen 0 10