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Neosmilaster Georgianus» from Anvers Island, Antarctica Costs of brood maintenance and development in the seastar Neosmilaster georgianus from Anvers Island, Antarctica MARC SLATrERY, Department of Biology, University ofAlabama, Birmingham, Alabama 35294 ISIDRO BOSCH, Department of Biology, State University of New York, Geneseo, New York 14454 arental investment of marine inver- ptebrates that protect their offspring through development to a juvenile 600 BW stage (that is, brooders) includes both direct and indirect energetic costs. 450 Direct costs, for instance, might include the energy initially allocated to eggs as provisional reserves for development 300 (Turner and Dearborn 1979) or to pro- duce larger juveniles (Lawrence, 150 McClintock, and Guille 1984). Indirect energy costs might include a reduced capacity to feed while holding a brood 0 or even starvation in cases where E females carry broods in their oral cavi- 1000 PC ties and are prevented from feeding 0 (Emlet, McEdward, and Strathmann 750 1987). 0 The total energy costs associated CL with brood protection will be related to 500 the duration of the brooding period. Slow developmental rates and pro- 250 longed periods of brood protection are E well-known characteristics of antarctic C) invertebrates (Pearse, McClintock, and 0 Bosch 1991). Therefore, a relatively high cost of reproduction might be 40 Fer expected in this fauna. The purpose of this study was to examine the costs of brooding and brood development in 30 the seastar, Neosmilaster georgianus. These large (having a radius of 51.4 20 centimeters) forcipulate asteroids are widespread in shallow subtidal com- 10 munities of the Antarctic Peninsula (Dearborn and Fell 1974). Neosmilaster georgian us exhibits reproductive asyn- 0 chrony within populations, an unusual 0 1 2 3 4 5 pseudocopulatory spawning behavior, Brood Stage and extended periods of brood protec- -0--ash tion during which the female is unable -0-- carbohydrate to feed (Slattery and Bosch in press). lipid Collections of Neosmilaster geor- A protein gianus were made, during the 1991 field - remainder season at Palmer Station, from depths of 2-15 meters (m). Wet and dry weights of the whole body, body wall, Figure 1. Biochemical composition of the body wall (BW), pyloric caeca (PC), and gonad (G) for brooding Neosmilaster georgianus females throughout brood stages 1 to 5. Stage 0 individuals pyloric caeca, and gonads of 31 female indicate a prespawned condition. Each point represents the mean ±1 standard deviation (N=7, and 5 male seastars were measured. 5, 5, 7, 1, and 6 for stages 0 to 5, respectively). ANTARCTIC JOURNAL - REVIEW 1993 136 Wet organ indices (ratio of wet body components to the may have a lower frequency of reproduction compared to whole body) were determined for all individuals. The percent- their temperate and tropical counterparts, which typically age of biochemical composition (ash, carbohydrate, lipid, and produce annual broods. protein) of the dry body components was also determined Broods of all females were removed, counted, and cate- using methods detailed in Lawrence and Guille (1982). The gorized into one of five groups based on developmental stage. energetic content of the different body components was (Prespawned individuals were classed a stage 0.) Broods were determined from the tissue biochemical composition using dried and ashed for organic composition, lyophilized for bio- energy-equivalent coefficients calculated by Brody (1945). chemistry, or fixed for sectioning. Samples were weighed on a The energetic content of females holding each brood stage Cahn microbalance prior to and after ashing in a muffle fur- was compared to determine costs associated with brooding- nace, and the organic weight was determined by subtraction induced starvation (figure 1). (figure 2). Biochemical tests were conducted on pooled whole The stage-specific energy content of the body wall, embryos and juveniles, of like developmental stage, to pro- pyloric caeca, and gonads of females holding broods was vide adequate sample weights for analyses. Thin-sections compared to estimate the costs associated with brooding- were examined via light and transmission electron induced starvation. There were no significant changes in the microscopy to determine the purpose of an amorphous mem- composition of the body wall. Lipid levels in the pyloric caeca, branaceous tubule interconnecting individuals within all the principal storage organ of seastars, were initially twice stage 2 broods. that reported in temperate and tropical species and compara- Brooded individuals exhibited a significant (P<0.0001) ble to other antarctic seastars (Lawrence and Guille 1982; increase in dry weight with a coincident significant (P<0.004) McClintock and Pearse 1987). All biochemical constituents decrease in organic weight during development from stages 1 and the energy content within the pyloric caeca exhibited sig- to 5. These overall changes were consistent with a trend for nificant (P<0.001) declines with stage of brood development, decreased lipid and protein during the onset of ossification ; an indication that nutrients were being redistributed to other (stage 4 and 5) in the developing offspring (data not shown). A parts of the body. In temperate seastars, a major part of these slight increase in organic weight, lipid content, and conse- energy reserves is allocated to the production of new eggs in quently energy levels occurred in early development (stage 1 J preparation for the next reproductive event (Chia 1969). In N. to 3), though this change was relatively small compared to the • georgianus, the stage-specific lipid content of the gonads of losses that occurred during the ossified stages. These results brooding females did not change significantly after spawning suggest, in contrast to antarctic echinoderm embryos exam- (figure 1) nor was there significant growth of existing, early- ined by Lawrence, et al. (1984), that N. georgianus produces stage oocytes (Slattery and Bosch unpublished data). Thus, large eggs in part to offset energetic demands of develop- the resources of the pyloric caeca are utilized for maintenance ment. These early embryonic changes were coincident with during the long brood cycle (approximately 1 year) and not in the development of membranaceous tubules that effectively preparation for future reproductive events. On the basis of the joined brood mates, forming clusters of up to 40 individuals. extended periods required for oocyte production in antarctic Histological evidence showing the movement of lipid and echinoderms (18 months or more: Pearse, McClintock, and other material through these tubules suggest they are a means Bosch 1991), we predict that species such as N. georgianus of "cannibalizing" broodmates for energy to fuel develop- ment. A trend toward a 25 percent decrease in the numbers of siblings per brood between spawning and the separation of 4.0 brood clusters (stage 0 through 3) supports our interpretation of sibling cannibalism. In fact, similar structures connecting brood mates occur in a deep-sea asteroid, Leptasterias tenera 3.0 (Hendler and Franz 1982), and two antarctic seastars, Diplas- terias brucei and Notasterias armata (Bosch personal observa- tion), suggesting this unusual process of supplementing the initial parental investment in eggs is not be unique to N. geor- gianus. We wish to express our thanks to D. Karentz, T. Gast, and the Antarctic Support Associates personnel at Palmer Station for their support. J.M. Lawrence provided helpful editorial suggestions. This research was sponsored by National Science 0 Foundation grants OPP 90-17664 to D. Karentz and OPP 91- 1 2 3 4 5 18864 to J.B. McClintock. Brood stage References Figure 2. Neosmilaster georgianus juvenile growth throughout brood stages 1 to 5. Each point represents the mean ±1 standard devia- Brody, S. 1945. Bioenergetics and growth. New York: Hafner Publish- tion (N=10). ing. ANTARCTIC JOURNAL - REVIEW 1993 137 Chia, F.S. 1969. Histology of the pyloric caeca and its changes during tional Journal of Invertebrate Reproduction and Development, brooding and starvation in a starfish, Leptasterias hexactis. Biology 7(4), 249-257. Bulletin, 136(2), 185-192. McClintock, LB., and J.S. Pearse. 1987. Biochemical composition of Dearborn, J.H., and F.J. Fell. 1974. Ecology of echinoderms from the antarctic echinoderms. Comparative Biochemistry and Physiology, Antarctic Peninsula. Antarctic Journal of the U.S. 9(5), 304-306. 86B(4), 683-687. Emlet, R.B., L.R. McEdward, and R.R. Strathmann. 1987. Echinoderm Pearse, J.S., J.B. McClintock, and I. Bosch. 1991. Reproduction of larval ecology viewed from the egg. Echinoderm Studies, 2,55-136. Antarctic benthic marine invertebrates: Tempos, modes, and tim- Hendler, G., and D.R. Franz. 1982. The biology of the brooding seast- ing. American Zoology, 31(l), 65-80. ar, Leptasterias tenera, in Block Island Sound. Biology Bulletin, Slattery, M., and I. Bosch. In press. Spawning behavior of a brooding 162(3),273-289. antarctic asteroid, Neosmilaster georgianus. International Journal Lawrence, J.M., and A. Guile. 1982. Organic composition of tropical, of Invertebrate Reproduction and Development. polar, and temperate-water echinoderms. Comparative Biochem- Turner, R.L., and J.H. Dearborn. 1979. Organic and inorganic compo- istry and Physiology, 72B(2), 283-287. sition of post-metamorphic growth stages of Ophionotus hexactis Lawrence, J.M., J.B. McClintock, and A. Guffle. 1984. Organic level and (E.A. Smith) (Echinodermata: Ophiuroidea) during intraovarian caloric
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