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Brachiopoda
Brachiopoda
23
Phylum Brachiopoda
/. Emotby Pennington and Stephen A. Stricker
DEVELOPMENT
AND FORM
OF BRACHIOPOD
LARVAE
Craniacea
Craniacean development is described for Crania anoma h by Nielsen (1991), and we have included three of his
micrographs (Figures 23.4-C). The larva does not feed
and bears a general resemblance to articulate larvae (see
below). It develops an apical lobe and a mantle lobe
with three pairs of setal bundles. However, no pedicle
lobe is formed. Nielsen (1991) also describes the internal
structure of the larva. Metamorphosis is somewhat
peculiar. Adult Crania attach not by a pedicle but by
cementing the pedicle shell valve to the substrate. To
Phylum Brachiopoda
Articulata
The Articulata are the best-studied group of brachiopods
(reviewed by James et al., 1992), and embryos and larvae
of a number of species have been described (reviewed by
Chumg, 1990; Long and Stricker, 1991). Developmental
patterns within this group appear to be conservative, and
larvae of the species studied to date are similar. The
description here is based on Laqueus californianw and
Erebratalia transversa. These species are free-spawners,
but brooding has also evolved in many species of articulate brachiopods (reviewed by Chuang, 1990).
The characteristic articulate larva consists of an anterior 'apical lobe', a middle 'mantle lobe', and a posterior
'pedicle lobe' (Figures 23.5-7). These are not true segments, as in the setigerous larvae of annelids (Long,
1964). The apical lobe is ciliated overall, and in many
species develops a prominent band of locomotory cilia
around its circumference (Chuang, 1990). Anteriorly on
the apical lobe, an 'apical plate' bears an 'apical tuft' of
immotile cilia. These structures are presumably sensory
in function, but the apical tuft is lost prior to metamorphosis in a number of species including L.
californianus and I: transversa. Putative eye spots are
found on the apical lobe of some, but not all, species, as
are odd structures of unknown function called 'vesicular
bodies' which line the posterior margin of the lobe
(Figures 23.6A,B,E) (Long, 1964). The mantle lobe bears
four bundles of setae, and is unciliated in mature larvae
except for a band of cilia that runs anteroposteriorly
along its ventral surface (Figures zg.sA, 23.6B). The
pedicle lobe is also unciliated in mature larvae, and
develops a terminal concavity called the 'attachment
disk' (Figure 23.6B) (see Stricker and Reed, 1985a). All
443
Stricker, 1991), perhaps from the non-shelled early discinacean larva?Evolutionary speculations of this type are
explored further by Chuang (1991), Nielsen (1991) and
Freeman and Lundelius (1999).
LARVAL
LIFE AND SETTLEMENT OF
BRACHIOPOD LARVAE
Chuang (1968,1977,1990) observed the swimming behavior of plankcon-caught larvae in the laboratory. Unshelled
larvae swim without rotating, with the lophophore
directed fonvard. The larvae are propelled by cilia on the
cirri and median tentacle. Turning is accomplished by
bending the body in the esophagealregion, thereby pointing the lophophore in a new direction. The long early
larval setae are dragged behind. When disturbed, these
setae are erected to splay out in all directions in a probable
defensive reaction (Chuang,1977). Older shelled larvae
swim similarly, with the lophophore extended almost
entirely beyond the gaping shell valves (Figures 23.3D,E).
When viewed from the anterior end, shelled larvae rotate
dockwise while swimming.
Little else is known of the larval biology of discinaceans. Larvae have been taken in various of the
world's oceans, principally in the summer and fall
(reviewed by Hammond, 1980). Chuang collected larvae
of all developmental stages in surface plankton hauls.
However, Eichler (1911, reviewed in Chuang, 1968)
caught two discinacean larvae from 3000 m; these were
interpreted as mature (4 p.c.) drift larvae of the abyssal
species Pelagodiscus atlanticus. A few years later,
Ashworth (1915) caught similar larvae in the surface
waters of the Indian Ocean, from which he inferred
that the larvae of I! athntim must be capable of migrating to shallow water from abyssal depths. However, it
now seems possible that Ashworth captured the larvae of
a shallow-water discinian such as Discinisca, which is
relatively common in the Indian Ocean.
Phylum Brachiopoda
ACKNOWLEDGEMENTS
We thank the brachiopod experts who generously contributed photographs, K. Carlson, J. Fink, and A.
Gough who prepared the figures, and J. Barry, J.
Connor, and the David and Lucile Packard Foundation
who supported compilation of this chapter.
A t l a s of M a r i n e I n v e r t e b r a t e L a r v a e
Percival, E. (1960). A contribution to the life-history of the brachiopod Tegulorbymhia nigricam. Quart. /. Micro. Sci, 101,
439-458.
Raup, D.M. (1979). Size of the Permo-Triassic bottleneck and its
evolutionary implication. Science ~~6,217-218.
Rowell, A.J. (1960). Some early stages in the development of the
brachiopod C m i a anomala (Mueller). Ann. Mag. Nat. Hist.,
Sn: I3.3,328-333.
Rudwick, M.J.S. (1970). Living and Fossil Brachiopodr,
Hutchinson, London.
Stanley, S.M. (1977). Trends, rates and patterns of evolution in
the bivalvia. In Patterns of Evolution (ed. A. Hallam), pp.
zopz50. Elsevier, Amsterdam.
Strathmann, R R (1978). The evolution and loss of feeding larval
stages of marine invertebrates. Evolution 32,894306.
Stricker, S.A. (1999). Brachiopoda. In Encyclopedia of
&production (eds E. Knobii and J.D. Neill), vol. I, pp. 382-388.
Academic Press, London.
Suicker, S A and Reed, C.G. (1985a). Development of the pedid e in the articulate brachiopod Tmbratalia tramversa
(Brachiopoda, Terebratulida). Zoomo?phology 105,253-264
Suicker, S.A. and Reed, C.G. (1985b). The ontogeny of shell
secretion in Tmbtlrtaliammvma (Brachiopoda, Articulata). I.
Development of the mantle. /. Morph. 183,233-250.
Stridrer, S.A. and Reed, C.G. (1985~).The ontogeny of shell
transversa (Brachiopoda, Articulata).
secretion in T&a&
11. Formation of the protegulum and juvenile shell. /. Molph.
183, 251-272.
Thayer, C.W. (1986). Arc brachiopods better than bivalves?
Mechanisms of turbidity tolerance and their interaction with
feeding in articulates. Paleobiology 12,161-174.
Valentine, J.W. and Jablonski, D. (1983). L a d adaptations and
patterns of brachiopod diversity through time. Evolution 37,
1052-1061.
Vermeij, G.J. ( 1 9 ~ )The
. Mesozoic marine revolution: evidence
from snails, predators and grazers. Pakobiology 3,245-258.
Williams, A. and R o d , A.J. (1965). Brachiopoda - anatomy and
morphology. In Tnatise on Znucrtek PakontorogK Part H,
Bmhiopo& (4.RC. Moore), pp. 6138. GeologicalSociety of
America and University of Kansas Press, New York and
Lawrence, Kansas.
Williams, A, James, M A , Emig, C.C., Maclay, S. and Rhodes,
M.C. (1997). Anatomy. In Tmtise on I n v r r t e b PalcontologX
Part H, Bmchiopodz (ad. RL. Kaesler), pp. 7-188. Geological
Society of America and University of Kansas Press, Boulder,
Colorado and Lawrence, Kansas.
Yatsu, N. (1902). On the development of Lingukz attuti~.
/. ColL
Sci. Imp. Univ. Tokyo I~,I-112.
Zimmer, RL. (1973). Morphological and developmental afhities
of the lophophorates. In Living and FossiI Bryoma (ed. G.P.
Larwood), pp. 593-599. Academic Press, New York
--
B
J!
4-48
FIGURE 23.1
450
FIGURE 23.2
Lingulacean development
A. Recently hatched larva of Glottidiapyramiciata at the 3 p.c. stage, 6-7 days old. The shell valves
are 'embryonic' and formed prior to hatching; larval shell is not yet apparent. The mouth,
esophagus, and stomach are visible. Scale bar: 140 pm. (Reproducedwith permission from
Paine, 1963.)
B. Larva of Glottidia sp. with 5 p.c., from the plankton off Florida. Cirri are partially extended;
the median tentacle, epistome, gaping mouth, esophagus, and stomach are all visible.
Substantial growth of larval shell has occurred. Scale bar: 140 pm. (Photograph by Craig M.
Young.)
C. Lingukz anatina larva from Singapore with 7 p.c. Statocysts are visible near anterior border of
stomach. Scale bar: 130 p.(Photograph by Shou Hwa Chuang.)
D. Lingukz anatina larva with 9 p.c. Coiled pedicle is visible posterior to stomach. Scale bar: 260
pm. (Photograph by Shou Hwa Chuang.)
E. Post-larva (juvenile) of Glottidiapyarnihta from the Gulf of Mexico. Pedicle has been everted
from shell and pedicle tip has become bulbous. Fringing mantle setae have developed. Scale
bar: 280 pm. (Reproduced with permission from Paine, 1963.)
F. Oblique view of gaping valves and extended lophophore of a swimming Lingukz anatina larva
with 7 p.c. Sale bar: 260 pm. (Photograph by Shou Hwa Chumg.)
G. Dorsoventral view of swimming 6 p.c. larva of L. anatina, with lophophore I l l y extended
beyond shell valves. Note the gaping mouth. Scale bar: 260 p.
(Photograph by Shou Hwa
Chuang.)
~ a i t Setae
~e
Pedicle tip
..
452
FIGURE 23.3
A. Shelled larva of Discinisca sp. from the plankton at the 4 p.c. stage. Median tentacle is visible,
as are non-articulated shell valves, and curved 'principle larval setae'. Scale bar: 200 p.
(Scanning electron micrograph by Claus Nielsen.)
B. Early larva of Discinisca sp. at the 2 p.c. stage, pressed between slide and coverslip. Median
C.
D.
E.
G.
H.
tentacle and two cirrus buds are visible, as are the two bundles of early larval setae. Shell valves
have not yet developed. Although not visible, the gut is complete and hctional at this stage.
(Reproduced with permission from Chuang, 1977.)
Scale bar: IOO p.
Dorsal view of early Discinisca sp. larva at the 3 p.c. stage in swimming posture. Lophophoral
cirri are spread laterally and the mouth is gaping. The esophagus, stomach, and larval setae
hang below and are dragged behind. Supposed eye spot is on right side of stomach (see text.)
Scale bar: IOO pm. (Reproduced with permission from Chuang, 1977.)
Dorsal view of Discinisca sp. larva at the 4 p.c. stage, in swimming posture. Median tentacle,
mouth, esophagus, stomach, and early larval setae are visible, as is the developing larval shell.
Scale bar: IOO pm. (Photograph by Shou Hwa Chuang.)
Ventral view of shelled 4 p.c. larva of Discinisca sp. in swimming posture. The long, straight
early larval setae have been lost but replaced by curved 'principle larval setae' hanging beneath
the shell valves, and 'looped flexible setae' faintly visible within the mantle cavity to either side
of the esophagus and stomach. The developing pedide is just visible as a transparent oval
immediately posterior to the stomach. Scale bar: 200 pn. (Photograph by Shou Hwa Chuang.)
Shelled larva of Disknisca sp. at the 4 p.c. stage. Shell valves are rotated showing lack of
articulation; the ventral valve has a concave 'bay' in outline. The pedicle bud is visible, as are
several types of larval setae. Scale bar: 200 pm. (Reproduced with permission from Chuang,
1977.)
Post-lama of Discinisca sp. at the 5 p.c. stage, 4 days after settlement in the laboratory. The
median tentacle is undergoing atrophy, and the long definitive setae are well developed. Scale
bar: 200 pm. (Photograph by Shou Hwa Chumg.)
Low magnification lateral view of 4 p.c. larva of Discinisca sp. in swimming posture, showing
length of early larval setae. Scale bar: IOO pm. (Reproduced with permission from Chuang,
1977.)
Median Tentacle
Cil
Shell Valves
Larval Setae\
Principal
Larval Setae
Median
Girri /~entacle
Stomach f
"
Definitive
Setae
Principal
Larval Setae
Dorsal
Valve
veAtra~
Pedicle Valve
Bud
454
FIGURE
23.4
..-Apical Lob
a-
Locomotory --,
Ciliated
Band
Mantle Lobe
FIGURE 23.5
Ventral Ciliated
orsal Setal
undle
Setal Bundle
I.
458
FIGURE 23.7
cdforniauu
k Oblique ventral view of late gastrula or 'wedge' stage. The apical tuft of cilia is forming (poorly
B.
C.
D.
E.
visible) at the new anterior end of the gastrula, on the upper right. The gastrula is undergoing a
change in swimming axis such that the blastopore, which was posterior, is becoming
posteroventral, and is dosing. Scale bar: 50 pm. (Scanning electron micrographs A-D and F
reproduced with permission from Pennington et al., 1999.)
Oblique dorsal view of lobe formation in an early larva. Anterior is at top. The blastopore faces
away from the viewer and has closed. The larva is dividing into apical, mantle, and pedicle
lobes, and the four bundles of latval setae have formed. Apical Nft is present but has been lost
in this specimen. Scale bar: 50 pm.
Dorsal view of young larva. The apical tuft of cilia is prominent; the larval setae are still short,
and the pedide lobe is still ciliated and rounded in outline. Scale bar: 50 pm.
Lateral view of larva in the process of metamorphosis. Pedide lobe is attached to substrate and
mantle lobe is retracting anteriorly to cover the apical lobe. Larval setae are splayed laterally.
Scale bar: 50 pm.
Anterior-on view of L. calzj%vzianw undergoing metamorphosis. Mantle lobe has mostly
retracted to cover the apical lobe, and larval setae project anteriorly. Groove in ventral side of
apical lobe may represent forming stomodeum or esophagus. Shell valves not yet obvious. Scale
bar: 50 pm. (Scanning electron micrograph by J.T. Pennington.)
Metamorphosed juvenile. The apical lobe is now covered by the mantle and shell valves, and
larval setae project anteriorly from the gape between valves. Lophophoral cirri are not clearly
formed. Scale bar: 50 p.