Chapter

23

Phylum Brachiopoda
/. Emotby Pennington and Stephen A. Stricker

Brachiopods or 'lamp shells' are sedentary ater-feeding invertebrates that superficially resemble the bivalved mollusks (see Rudwick, 1970). However, basic features of their anatomy (body axes, gii, foot, gonads) are h d a mentally different from those found in bivalves, and brachiopods have often been considered to be evolutionarily unrelated to the Mollusca (see Brusca and Brusca, 1990). About 30 ooo species and 120 genera of brachiopods have been described from a fossil record which extends into the lower Cambrian (Rudwidc, 1970; James et al., 1992). During the Paleozoic, brachiopods were both diverse and exceedingly abundant (Thayer, 1986). T h i i proliferation ended about 250 million years ago during the Permo-Triassic extinction, wherein perhaps 95% of all marine species were eliminated (Raup, 1979). Brachiopods did not rediversify following this event (Stanley, 1977; Vermeij, 1977; Thayer, 1986). Today, 300 or so species of brachiopods remain. Historically, the group has been well studied by paleontologists but neglected by biologists. This imbalance has begun to improve, in part because of interest generated by recent molecular phylogenies that ally the brachiopods with the protostome phyla in spite of their classical placement with the deuterostomes on morphological and developmental grounds (see Zimmer, 1973; Brusca and Brusca, 1990; Cohen and Gawrhrop, 1997; Lueter and Bartolomaeus, 1997),Tht general biology of brachiopods has been recently reviewed by James et al. (1992) and various chapters of the revised Treatise of Invertebrate Palcontology (e.g. Kaesler, 1997). Brachiopod reproductive biology, including gametogenesis and embryology

have been reviewed by Chuang (~ggo), Long and Stricker (1991) and Suicker (1999) and therefore will not be dealt with in the present chapter. We describe and illustrate the diversity and beauty of larval stages of all major groups of brachiopods. For practical purposes, we follow Nielsen (1995) and present the l a d forms as representatives of four main groups of living brachiopods: Lingulacea, Diinacea, Craniacea, and Articulata. The first three of these taxa are traditionally taken as superfamilies within the class Inarticulata, opposite the class Articulata (Williams and Rowell, 1965).The reader should be aware, however, that this scheme is subject to debate, which we do not wish to enter into here (reviewed by Carlson, 1995). Brachiopod larvae have no special names.

DEVELOPMENT AND FORM

LARVAE

OF BRACHIOPOD

The Lingulacea are composed of two living genera, Linguka and Glattidia,whose larvae are very similar. Yatsu (1902) and Freeman (1995) present descriptions of development within the group; Yatsu's monograph, in particular, contains many beautiful l i e drawings of L. anatim embryos and larvae. The main features of the Lingulacea are dorsal and ventral shell valves underlain

by mantle tissue, a complete gut, a developing pedicle,

and a lophophore (Figures 23.1 and 23.2). Each shell valve is divided into a posterior semicircular 'embryonic shell' or 'protegulum', which develops before a larva hatches from its egg membrane, and a larger, circular to

Atlas o f Marine Invertebrate Larvae

ovoid 'larval shell', which is added as larvae grow in the plankton. For the ligulaceans, we have followed the shellnaming convention of Chuang (1977) and Williams et al. (1997): protegulum or embryonic shell, followed by larval shell, then post-larval shell. The lophophore consists of pairs of cirri that bud off sequentially on either side of the 'median tentacle', so that the youngest tentacle pair is most anterior (Figure 23.1B, cirrus 13). Lingulacean larvae are staged by counting the number of pairs of cirri (abbreviated 'P.c.'); e.g., a larva with four pairs of cirri plus a pair of well-formed cirrus buds is termed a '5 p.c. larva' (Chuang, 1959, 1990). The median tentade is a putative sensory organ characteristic of lingulacean and discinacean larvae (Hay-Schmidt, 1992; Lueter, 1996). The anterior lip of the mouth is termed the 'epistome'. This structure has received much attention, as it has been suggested that it represents the prosome in a trimerous deuterostome body plan (see Zimmer, 1973; Brusca and Brusca, 1990, but also Lueter, 1996). Paine (1963) published a developmental sequence of Glottidia pyramidata larvae, and we have supplemented his series with previously unpublished images of Glottidia spp. and L. anatina larvae from the plankton (Figure 23.2). Lingulacean eggs are spawned into the plankton. Embryonic development takes place within an egg membrane, from which young larvae hatch at the 2 p.c. stage (Chuang, 1990), with gut and embryonic shell complete. The planktonic larvae feed and grow, adding cirri and a larval shell (Figures 23.2A,B) Statocysts form to either side of the esophagus at about the 5 p.c. stage (visible in the 7 P.C. larva in Figures 23.2C) (Chuang, 1990). By 7 7 p.c., the pedicle begins to differentiate posterior to the stomach (Figures 23.2D,E), and fine setae appear at the mantle margins (faintly visible in Figure 23.2D; Yatsu, 1902). Both Linguka and Glottidia larvae can attach to the bottom by their pedicles and burrow, once they have reached the 9 or 10 p.c. stage (reviewed by Chuang, 1990), thus becoming juvenile brachiopods. Among lingulaceans, there is no clear metamorphosis upon assumption of benthic life, although the pedicle is everted from the shell. The end of the pedicle becomes bulbous and sticky, the mantle setae enlarge, and the median tentacle atrophies (Figure 23.2E; Brooks, 1879; Yatsu, 1902; Paine, 1963). This lack of a striking morphological metamorphosis caused Long and Stricker (1991) to consider the 'larvae' described above as planktonic juveniles.
Discinacea

'Mueller larvae'. This name has been abandoned, and is now used for the larvae of turbellarian flatworms (Brusca and Brusca, 1990).The mature discinacean larva is similar to the lingulacean larva described above. Its main features are a bivalved, unhinged larval shell (protegulum is absent), a lophophore with median tentacle (Figure 23.3), a complete gut, and a pedide bud (see below and Chuang, 1990). Pigment spots have been reported in discinacean larvae, but whether or not these are actually eye spots remains questionable (Chuang, 1977). Chuang (1977) published a developmental series of Discinisca spp. larvae obtained from the plankton near Singapore. Young discinacean larvae do not resemble lingulacean larvae, at least superficially. Relative to the lingulaceans, shell growth is retarded. Larvae at the 2 p.c. stage (Figure z3.3B) lack shells, and are instead characterized by two bundles of 3-5 long 'early larval setae' (Figures 23.3H) (Chuang, 1977; 1990). The ciliated lophophore is evident with its two pairs of cirri, cirrus buds, and median tentacle, and the gut is complete and functional. The larval shell valves are secreted at the 3 or 4 P.C.stages (Figures 23.3D,E). During the remainder of larval life, the shell valves continue to grow, but the lophophore remains at the 4 p.c. stage and the early larval setae are lost (Figures 23.3E,F). Three additional types of setae develop in the 4 p.c. shelled larva following loss of the early larval setae. These are the curved 'principle larval setae', the 'looped flexible setae', and the fine mantle 'late larval setae' (faintly visible in Figure z3.3E; seta nomenclature from Hammond, 1980).A pair of statocysts also develops lateral to the stomach in 4 p.c. larvae (not figured), and a pedicle bud appears just anterior to the embayment in the smaller ventral valve (Figures 23.3E,F). Settlement is believed to occur at the 4 p.c. stage (Chuang, 1990) and, as in lingulaceans, there is no striking metamorphosis. A larva caught in the plankton later settled in the laboratory (Figure z3.3G) (Chuang, unpublished observations). Over the ensuing 4 days, (I) long setae grew anterior to the mouth and lophophore, (2) another pair of cirri developed, and (3) the median tentacle began to degenerate.

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

Freeman (1999) has recently analyzed the embryology of Discinisca strigata, but Discinacean larvae are known mostly from the work of Chuang (1968,1977,1990) on Discinisca spp. larvae from the plankton. Chuang (1977) and Hammond (1980) review historical records of larval occurrence, in which these larvae are often referred to as

Phylum Brachiopoda

443

achieve this, the larvae flex ventrally into a U-shape, with apical lobe and the posterior of the mantle lobe in contact with the substrate, and the dorsal setae splayed out above (figured in Nielsen, 1991). Cementation is not well described, but Rowel1 (1960) believes the periostracum of the pedicle valve is used as cement; this valve is secreted by the posterior end of the mantle lobe (Nielsen, 1991). A brachial (dorsal) valve is secreted over the animal, and a lophophore, gut, and other adult structures differentiate. Nielsen (1991,1995) believes this articulate-like larva and the co-occurrence of calcareous shell valves should ally the Craniacea with the articulates, rather than with the Inarticulata. The latter is the traditionally accepted classification scheme based on the presence of a complete gut and the lack of shell articulation in adults. However, both Rowel1 (1960) and Chuang (1974) report that juvenile C. anomakz possess a median tentacle similar to that found in inarticulate larvae. Curiously, this characteristically 'inarticulate' structure is not present in larval C. anomakz.

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

articulate larvae lack functional guts and do not feed. Their internal organs tend to be poorly formed (Long and Stricker, 1991), but have been described in detail by ConMin (1902) and Long (1964). Brooded larvae (Figures 23.6D-F) are generally not much different from the free-swimming - larvae described above (Grobe and Lueter, 1999; reviewed by Chuang, 1990), although brooded stages appear to be less heavily ciliated. Pennington et al. (1999) presented a developmental sequence for Laquetls californianw. Gastrulae develop about 2 days after fertilization (Figure 23.7A). Over the next 2 days, the blastopore closes and the three lobes of the larval body differentiate (Figure 23.7B). The apical tuft and larval setae develop on their respective lobes (Figure 23.7C). The pedicle lobe remains bulbous and sparsely ciliated in young larvae. As larvae mature, the mantle lobe grows posteriorly and partly encloses the pedicle lobe (Figure 23.5A). At metamorphosis, the pedicle lobe attaches to the substrate (Stricker and Reed, 1~856)'. Several authors describe an initial, weak attachment, followed by permanent cementation (Chuang, 1996a). Muscular contractions then reverse the mantle lobe, so that it 'everts' to enclose the apical lobe (Figures 23.6C, 23.7D,E). The new external surfaces of the mantle lobe secrete the first shell valves (Figures 23.7E, F), typically within 24 h of cementation. These first shell valves are referred to as 'protegula' in articulate brachiopods and craniaceans, even though, unlike in the inarticulates, they are secreted after metamorphosis (Stricker and Reed, 1985b,c; Freeman and Lundelius, 1999). In both articulates and lingulaceans, the protegula lack growth lines (Freeman and Lundelius, 1999). Following metamorphosis, the mouth opens and the juvenile begins to feed. The spatial relationship between the sites of blastopore closure and mouth formation are not well described (see Nielsen, 1991, for a discussion of the phylogenetic implications of patterns of gut development). Several authors describe or figure ectodermal invaginations or folds in the apical lobe (Figure 23.7E) (citations in Pennington, 1999), which may represent an incipient esophagus or stomodeum. Because articulate gastrulae form but then close the archenteron (primitive gut), it would seem likely that the non-feeding articulate larvae are derived from a feeding type of larva (see Strathmann, 1978). Valentine and Jablonski (1983) suggest that articulate species with feeding larvae were lost during the Permo-Triassic extinction. They argue that the failure of the Brachiopoda to rediversify following the extinction is owing to a limited ecological and evolutionary potential of non-feeding developmental patterns. If articulate larvae once fed, did they resemble the feeding inarticulate larvae?Are the shelled inarticulate larvae themselves derived (e.g., are heterochronic juveniles cf. Long and

Atlas of Marine Invertebrate Larvae

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

opment of juvenile structures. Settlement of G. pynamih t a apparently occurs on unconsolidated sand bottoms; juveniles are subsequently transported by current to the dense adult populations which accumulate in seagrass beds (Paine, 1963). Life table calculations for G. p m i h t a indicate that one or two I-month-old juveniles are produced for each 10 ooo eggs spawned (Paine, 1963), a figure that reflects the mortality rate of larvae during 20 or more days in the plankton.

The natural history of lingulacean larvae is known mostly from the observations of Yatsu (1902) for L. anatina from Morioso Inlet, Japan, and those of Paine (1963) for G. pyramidata from Ahgator Harbor, Florida. In the laboratory, L. anatina larvae swim upward with shell hanging beneath the lophophore, with "cirri gracefully protruded out of the shell to almost two thirds of their length" (Yatsu, 1902) (see Figures 23.2B,F,G). When disturbed, larvae retract their cirri and sink. Paine (1963) made similar observations of G. pyramidata swimming behavior and additionally observed the larvae to be positively phototactic, though photoreceptors were not identified. Spawning seasons have been reviewed by Long and Stricker (1991) and James et a. (1992); Paine (1963) concluded that the breeding season of G. pyramidata is spring and summer but more restrictive at higher latitudes. Chuang (1959) found L. anatina larvae year-round near Singapore, Paine (1963) observed that spawning occurred during night-time high water on spring tides, resulting in a seaward flushing of embryos and larvae. He additionally found few larvae in turbid Alligator Harbor water, but high numbers were present in the clear water of the Gulf of Mexico. Within Morioso Inlet, Yatsu (1902) found larvae of 7 or more p.c. to be abundant during flood tide, but younger larvae always to be uncommon. Based on their respective observations, both Yatsu (1902) and Paine (1963) suggested that young stages are exported from inshore waters, and return when ready to settle on the mud flats. Chuang (1959) did not find a lunar periodicity to spawning in L. anatina near Singapore. Larvae of L. anatina and G .pyramidan were estimated to take 32 and 20 days, respectively, to reach early settlement stages (9 or 10 p.c.), addiig a new cirrus pair each 2-4 days (Yatsu, 1902; Paine, 1963). Larvae that do not encounter suitable substrate can remain in the plankton probably several additional weeks as 'drift larvae' (Figure 23.1), continuing to grow and add cirri to at least the 15 p.c. stage (reviewed by Chuang, 1990). Paine (1963) observed that drift larvae obtained offshore in clear water had delayed pedide and setal development, relative to larvae of similar stage but obtained nearshore, and suggested that proximity to sediment induced devel-

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.

Eggs of Crania anomala take 3 days to develop into larvae (Figures 23.4.14-C) (Nielsen, 1991). Swimming behavior has not been described, but it is known that larvae flex their setae in a defensive array when disturbed. When 4-day-old larvae become competent to settle, they begin crawling on the bottom, then attach and undergo metamorphosis. C, anomala does not brood, but craniacean developmental stages have not been collected from the plankton. Swedish C. anomah apparently spawn in the fall or winter (Nielsen, 1991), and Scottish C. a n o d are suggested to spawn in both

Phylum Brachiopoda

fall and spring (Rowell, 1960). Dispersal must be limited by a very short larval period, but nothing is known about larval depth distributions, drift larvae, substratum selectivity at settlement, l a d survival, or recruitment. In Scotland, Rowell (1960) documented a spring-time cohort of benthic juveniles in the 3 p.c. stage.
Articulata In the laboratory, young larvae of Laqueus calzjknianus swim about I mm s-I atthe surface ofcultures, spiraling clockwise (anterior view; Pennington et al., 1999). Larvae that contact the suhce or each other stop swimming and erect their seme. L. califmianus larvae do not have obvious ph~toreceptorsand do not respond to light, but photobehavior has been reported in a number of other articulate species (reviewed by Long and Snicker, 1991; James et al., 1992; Chuang, 1996a). The vertical swimming behaviors exhibited by L. cal@mianus are presumably geotactic, though articulate larvae lack statocysts. Mature larvae do not spiral, but swim downward or at the bottom of containers, with their ventral surface pressed against the substratum in an apparent searching behavior common to a number of brachiopod species (Chuang, 1990; 1996a,b). Gregarious settlement has commonly been reported for articulate larvae, and a few species have been shown to prefer grooves or concavities in the substratum as settlement sites (reviewed by James et al., 1992). Pennington et al. (1999) reported that larvae of L. calz$rnianus prefer to settle on the shells of living conspecific adults. 1 ) Jameset al. (1992) have Long and Stricker ( 1 ~ ~and summarized information on articulate reproductive seasons. Most species appear to spawn in fill and winter. Developmental periods of the non-feeding larvae are relatively short, typically a few days for free-spawning and apparently also for brooding species (Chuang, 1990; James et al., 1992). Peck and Robinson (1994) did, however, culture larvae of the Antarctic articulate LiotbyreIla uva for 45 days. Pennington et al. (1999) also maintained L. calz$rnianus larvae for 71 days in culture, although the latter species only requires 5-7 days to reach metamorphic competency. Except for Calloria incompicua in a tidepool (Percival, 1960), articulate larvae have not been taken in plankton collections (Chuang, 1990). Pennington et al. (1999) calculated that larvae of L. calz$rnianus could swim to the surface from the adult beds at IOO m in about 28 h. If the larvae remain near the surface for the next few days, dispersal on the order of tens of kilometers should be possible. Similar arguments could be made for any species with an upward-swimming larva that spends more than a few hours in the plankton. Larval survivorship has not been estimated for articulates. The benthic distributions of articulate juveniles are

often patchy, owing in part to substratum selectivity by the larvae upon settlement. A number of studies have documented population structures of articulates, including the apparent recruitment of larval cohorts into benthic populations (see e s w y Doherty, 1979; others reviewed by James et al., 1992).

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.

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B J!

Freeman, G. (1995). Regional specification during embryogenesis in the inarticulatebrachiopod Glonidia. Drv. BwL 1p,15-36. Freeman, G. (IW). Regional qeci6cation during embryogenesisin the inarticulate b&opod ~ i z c i n k a Dm Bwlzo9,321j39. Freeman, G. and Lundelius, J.W. (1999). Changes in the timing of mantle fbrmation and l a d life history traits in liguliform and craniiiorm brachiopods. Letbaia 3 5 197-217. Grobe, P. and Lueter, C. (1999). Reproductive cycles and l a d morphology of three recent species of Argyrotheca (Terebratellacea: Brachiopoda) from Mediterranean submarine caves. Mar. BwL 134,595400. Hammond, L.S. (1980). The larvae of a discinid (Brachiopoda: Inarticulata) from inshore waters near Townsville, Australia, with revised identification of previous records. /. Nat. H . . q, 647-661. Hay-Schmidt, A. (1992). Ultrasuuccure and immunocyochemistry of the nervous systun of the larvae of Lingukz amtinu and Glotcidia sp. (Brachiopoda). Zoomotphology I & 18pzos. James, M A , Ansell, A.D., Collins, M.J., Curry, G.B., P& L.S. and Rhodes, M.C. (1992). Biology of living brachiopods. Adv. Mar. BioL 28,175-387. Kaesler, RL. (1997). Tnatise on ZnuerrebraK Pakontoba Part H, Bmhiopok (ed. RC. Moore). GeologicaJ Society ofAmerica and University of Kansas Press, Boulder, Colorado and Lawrence, Kansas. Long, A.J. (1964). The Embryology of Thne Speck Representing Three Supefamilies of A r h h t e Brachiopodz PhD thesis. Zoology Department, Universityof Washington, Seattle, Washington. Long, J h and Striker, S A (1991). Brachiopoda. In Reprothuh in Marine Invertebrates, %L 6, ~chinodmns and~opho~horates (eds A.C. Giese. J.S. Pearse and V.B. Pearse), pp. 47-84. Boxwood Press, Palo Alto, CA. Lueter, C. (1996). The median tenmde of the larva of Lingula anutinu (Brachiopoda) from Queensland, Australii. Aust. 1 . ~ ~ o L M 355-366. , Lueter, C. and Bartolomaeus, T. (1997). The phylogenetic position of Brachiopoda, a comparison of morphological and mokadar data. ZooL Smpta 26,245-253. Nielsen, C. (1991). The development of the brachiopod Crania (Neocrania) anomala (O.F. Mueller) and its phylogenetic significaace. Acta Zwl. (Stock.) p, 1-23. Nielsen, C. (1995). Animal Evolution: Interrelationships of the Living Phyla Oxford University Press, Oxford. Paine, RT. (1963). The ecology of the brachiopod Glonidiapamidata. EcoL Monogr. 33,187-213. P& L.S. and Robinson, K. (1994). Pelagic larval development in the brooding Anmrctic brachiopod LiothynIla uva. Mar. Bwl 120,279-286. Pennington, J.T., Tamburri, M.N. and Barry, J.P. (1999). Development, temperature tolerance, and settlement prekrence of embryos i d larvae of the articulate brachiopod W u e u s calr~rnianus. BwL B d 196,245-256.

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 & a & transversa (Brachiopoda, Articulata). secretion in T 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

4-48

Atlas o f Marine Invertebrate Larvae

FIGURE 23.1

Larva of the lingulacean Glottidia spp.

A. Late-stage larva of G l o t h ' d i a sp. collected from the plankton off the east coast of Florida, U.S.A.
Latvae with 9-10 pairs of lophophoral cirri are competent to settle to the benthos; a larva with t h i i many cirri has not encountered a benthic substrate and is termed a 'drift larva' (see text). S d e bar: 280 pm. (Photograph by William B. JaecMe.) B. Line drawing of the lingulacean larva in A. Dorsoventral view, with shell valves lying flat on a microscope slide. Cirrus pairs are numbered; new cirri are added sequentially to each side of the median tentacle. Lingulacean and discinacean larvae are staged by counting pairs of cirri; this larva is at the '13 p.c.' stage. Statocysts are not visible, and are apparently being obscured by the anterior portion of the stomach. Similarly, the intestine is not visible, but it runs along the righthand side of the stomach in lingulacean larvae. The embryonic shell of Glottidia pyramidata from Florida is 280 pm wide and is M y formed upon hatching; the larval shell grows as the larva feeds in the plankton and in this specimen is probably about 1.2 mm wide. (Drawing by Kirsten Carlson.)

450

Atlas o f Marine Invertebrate Larvae

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

Atlas o f Marine Invertebrate -Larvae

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
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.)

C.

D.

E.

G.

H.

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

Atlas o f Marine Invertebrate Larvae

FIGURE

23.4

Larvae of Crania anomah from Sweden

A. Dorsal view, showing apical lobe and mantle bearing larval setae. There is no pedide lobe. Scale bar A X : s o pm. (Scanning electron micrographsA-C reproduced with permission fiom
Nielsen, 1991.) B. Ventral view of larva of C. anomah. C. Lateral view. During metamorphosis, the larva will contract into a U-shape with setae up and

..-Apical Lob

a-

Locomotory , Ciliated Band

Mantle Lobe

Atlas o f Marine Invertebrate Larvae

FIGURE 23.5

Larva of a representative articulate brachiopod, L a q m caGifbrnianus

A. Lateral view of a mature lama. This species lives at a depth of IOO m in Monterey Bay,
California. Scale bar: 50 pm. (Scanning electron micrograph reproduced with permission from Pennington et d.,1999.) B . L i.e .d . r a ~ showing g ~ $ i & ~ e , s , t + 1 1 ~ ~ & ~ 4 ~ ~by D .=te~ r a w i n_Carb?n.) ~

Ventral Ciliated

orsal Setal undle

Setal Bundle

I.

458

Atlas of Marine Invertebrate Larvae

Larvae of free-living and brooded articulate brachiopods

A. Young larvae of Tmbratalia transwenu, from the San Juan Islands, Washington. These larvae have an apical tuft of cilia and rounded or bulbous pedide lobes without attachment disks. Also visible are the 'vesicular bodies' along the posterior margin of the apical lobe, and the dorsal and ventrolateral s e d bundles. Scale bar: IOO pm. (Scanning electron micrograph reproduced with permission from Stricker and Reed, 198~a.) B. Mature larva of I: transversa By this stage, larvae lose the apical tuft of cilia (concavity demarking the apical plate still visible). They develop a transverse ring of locomotory cilia at the posterior end of the apical lobe, and a longitudinal band of cilia on the ventral surface of the mantle lobe. The mantle lobe also grows posteriorly, to partially enclose the pedicle lobe, and the concave 'attachment disk' forms at the posterior end of the pedicle lobe. Scale bar: 50 pm. (Scanning electron micrograph reproduced with permission from Strider and Reed, 1985a.l C. Recently metamorphosed juvenile of I: tmnswena Mantle lobe has reversed toward anterior to cover the apical lobe and has secreted the protegulum. Mantle lobe s e d bundles now project from the gape of the forming shell valves. The apical lobe is not visible but the stomodeum and first cirri are presumably differentiating. The pedicle lobe is flattened at its distal end where it was attached to the substratum. Scale bar: 50 pm. (Scanning electron micrograph reproduced with permission from Stricker and Reed, 1985c.) D. Five brooded larvae of the Mediterranean articulate brachiopod Awotheca cuneata within the enlarged nephridial brood pouch of the adult. Scale bar: IOO pm. (Scanning electron micrographs D-F reproduced with permission from Grobe and Lueter, 1999.) E . Detail of brooded A. cuneata larva. Note the 'vesicular bodies' at the posterior margin of the apical lobe and the midventral longitudinal band of cilia on the mantle lobe. Scale bar: 40 pm. P. Larva of A. corhta removed from brood pouch. As in non-brooded larvae, the ventral side of the mantle lobe has grown down to cover most of the pedide lobe; the midventral longitudinal band of cilia is also apparent. Scale bar: 60 p.

Atlas o f Marine Invertebrate Larvae

FIGURE 23.7

La&ae of the articulate brachiopod Laq-

cdforniauu

k Oblique ventral view of late gastrula or 'wedge' stage. The apical tuft of cilia is forming (poorly
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.

B.

C.

D.

E.