Palatability and Chemical Defense of Eggs, Embryos and Larvae of Shallow-Water Antarctic Marine Invertebrates

MARINE ECOLOGY PROGRESS SERIES Published July 31 Mar Ecol Prog Ser Palatability and chemical defense of eggs, embryos and larvae of shallow-water antarctic marine invertebrates James B. ~~Clintock'~',Bill J. ~aker~ 'Department of Biology, University of Alabama at Birmingham, Birmingham, Alabama 35294-1170, USA 2Department of Chemistry. Florida Institute of Technology, Melbourne. Florida 32901. USA ABSTRACT: The present study examines aspects of palatability and chemical defense in the early life history stages of 7 common species of shallow-water antarctic marine invertebrates with contrasting modes of reproduction. These included the spawned eggs and larvae of a sea urchin and the intrao- vanan eggs of a sea star, both with planktotrophic larvae, and the lecithotrophic embryos and larvae of 3 sea stars with elther brooding 01- broadcast~ngmodes of reproduction. In addition, a sponge and a nudibranch with brooded lecithotrophic embryos and egg nbbons, respectively, were investigated. Ovaries containing eggs, spawned eggs, and developing embryos or larvae were tested for their palatability against 3 common sympatric predators representing widely disparate feeding patterns: the sea star Odontaster vahdus [d benthic scavenger), the sea anemone Isotealia aritarctlca (a benthic filter feeder and opportunistic carnivore) and the amphipod Paramoera walkeri (a benthic and water column scavenger). Alginate feeding pellets containing hydrophilic and lipophilic extracts of spawned eggs of the broadcasting planktotrophic sea urchin Sterechinus neumayeri and ovaries containing developing eggs of the broadcasting planktotrophic sea star 0. validus were readily consumed by all 3 predators. Pellets containing hydrophilic and lipophilic extracts of 4-armed echinoplutei larvae of S. neumayeri offered to the sea anemone I. antarctica were also consumed, indicating a lack of chemical defense. In contrast, at least 1 of the 3 predators demonstrated feeding inhibition to eggs, embryos, larvae or their hydrophilic or lipophilic extracts in the remaining 5 lecithotrophic species. In the lecithotrophic sea star Diplasteria brucei we demonstrate that the basis of rejection is chemically mediated. It is likely that rejection among the other 4 lecithotrophic species is also chemically based as eggs, embryos and larvae are conspicuous and high in energy content, lack morphological defenses, and are immobile or sluggish swimmers Our findings Indicate predators display species-specific feeding deterrent responses and support observations that lecithotrophic embryos or larvae may be particularly well suited to chemical defenses. Chemical defense in early life history stages may be especially important in shallow antarctic seas where species with lecithotrophic development patterns are relatively common, and where conspicuous yolky embryos or larvae may spend a considerable period of time developing in benthic or pelagic environments prior to recruitment. KEY WORDS: Chemical defense . Antarctica Planktotroph . Lecithotroph . Embryo . Egg INTRODUCTION al. 1992, Lindquist 1996, Lindquist & Hay 1996). No ecologically relevant information is available for early Little information is available on the palatability and life history stages of polar marine invertebrates chemical defense of marine invertebrate eggs, em- (McClintock & Vernon 1990). Such information is bryos or larvae (Bakus et al. 1986, Paul 1992, Pawlik important because models for the evolutionary selec- 1993, Hay 1996),other than several studies examining tion of life history patterns in marine invertebrates temperate and tropical marine invertebrate larvae make assumptions about patterns of mortality of off- (Lucas et al. 1979, Young & Bingham 1987, Lindquist et spring (Mileikovsky 1971, Vance 1973, Strathmann & Strathmann 1982, Jablonski & Lutz 1983, Strathmann 1985, Emlet et al. 1987, Roughgarden et al. 1988, 0 Inter-Research 1997 Resale of full article not permitted 122 Mar Ecol Prog Ser Roughgarden 1989, Alexander h Roughgarden 1996). common sympatric predators that employ a variety of These models generally assume that eggs, embryos feeding tactics. Where sufficient amounts of material and larvae are vulnerable to predators, and have pri- could be attained, organic extracts were tested in feed- marily considered marine invertebrates with plank- ing pellets to determine whether there was a chemlcal totrophic modes of development basis to feeding inhib~tion. Marine invertebrates display a variety of reproductive modes. Generally either large numbers of very small eggs are released into the water column where MATERIALS AND METHODS they become feeding planktotrophic larvae, or much smaller numbers of larger eggs are either protected Invertebrate species representative of a variety of (brooded) by the parent or held within an egg mass reproductive modes and that were sexually mature where they develop through non-feeding lecitho- during the antarctic austral spring (October and trophic embryonic or larval stages (Vance 1973).While November, 1996) were targeted for collections using less common, some marine invertebrates release large SCUBA. The common sea star Odontaster validus and yolky eggs, embryos or larvae into the water column, the common regular sea urchin Sterechinus neumay- where in temperate and tropical waters they typically eri, both with broadcasting planktotrophic modes of spend a short period of time before settlement (Strath- reproduction, were collected from 20 to 30 m depth in mann 1985). In shallow antarctic marine waters, brood- front of McMurdo Station (77"511S, 164"40'E) and ing was once thought to be the predcminant reprodiic- irorn 3 to iO m depth at Cape Evans (77"38'S, tive mode in marine invertebrates (Thorson 1950). 164" 24'E), respectively (see McClintock et al. 1988 More recently, evidence has been presented indicating and Brey et al. 1995 for map and descriptions of collec- that the incidence of pelagic development in antarctic tion sites). The remaining species examined had leci- +h,,+,.-..h:- --.I-- -. marine invertebrates is similar to that forlnd ir! temper- L.lVLlVfJlllC IIIUUC~ ui leproauction, lne sea stars ate and tropical marine waters (Pearse et al. 1991), and Diplasterias brucej (an external brooder) and Perk- that while non-feeding modes of development pre- naster fuscus (a pelagic lecithotroph) and the nudi- dominate (Jablonski & Lutz 1983), a surprisingly large branch Tritoniella belli (lays egg ribbons) were col- number of antarctic species release large yolky em- lected from 25 to 35 m depth near McMurdo Station at bryos into the water column (Pearse et al. 1991). Large Arrival Heights. The sponge Isodictya setifera (an eggs, embryos and larvae of marine invertebrates may internal brooder that has an abbreviated larval stage) be particularly vulnerable to predation (Lindquist et al. was collected in 33 m of water near Little Razorback 1992, Lindquist 1996, Lindquist & Hay 1996) and espe- Island (77"401S,163"24'E), while the sea star Psilaster cially so in shallow antarctic waters where develop- charcoti (a pelagic lecithotroph) was collected from mental rates are reduced by several orders of magni- 30 m depth at New Harbor (77"34'S, 163"35'E) on the tude (Clarke 1982, Bosch et al. 1987, Bosch 1989, Bosch western side of McMurdo Sound. & Pearse 1990, Pearse et al. 1991) resulting in offspring The predators employed in feeding assays were cho- spending months on the benthos or in the water col- sen so as to represent a variety of feeding modes and umn before becoming juveniles. A wide suite of were sufficiently abundant to represent a significant antarctic predators including filter feeders and water- predation threat to eggs, embryos and larvae. The column and benthic scavengers are likely to provide common omnivorous sea star Odontaster validus sufficient selection for the evolution, of defensive traits (radius = 5 to 7 cm) (McClj.ntock et al. 1988, McClin- in eggs, embryos or larvae While water-column Inver- tock 1994) was collected (n = 50 to 80) as indicated tebrate grazers can be spatially or temporally patchy, above. This species was selected because Dayton et al. they can be extremely abundant when present (Garri- (1974) describes it as an important 'larval filter' son 1991). The lecithotrophic eggs, embryos and lar- through which all settling larvae and early juveniles vae of antarctic marine invertebrates would be partic- must pass. Also collected from Arrival Heights (30 m ularly vulnerable as they are often conspicuous due to depth) were individuals of the extremely abundant fil- their large size (Bosch 1989, Pearse et al. 1991), lack ter feeding and opportunistically carnivorous sea the swimming ability of planktotrophic larvae (Bosch anemone Isotealia antarctica (n = 20; disc diameter 10 et al. 1987, Bosch & Pearse 1990), and are attractive to 12 cm) (Dayton et al. 1974). Swarms (n > 400) of the prey due to their high energy content (McClintock & common omnivorous amphipod Paramoera walkeri (2 Pearse 1986). to 5 mm length) were collected near Little Razorback The present study examines whether the intraovar- Island in 3 m depth by a diver using a small aquarium ian and spawned eggs, and developing embryos or lar- net (15 X 10 cm mouth; 3 swipes through the water col- vae, of a suite of antarctic marine invertebrates with umn collected over 700 ind.). These are both season- contrasting modes of reproduction are palatable to ally benthic or sea-ice associated and may also fill the McCllntock 8: Baker: Chemlcal ecology of antarct~c~nvertebrates

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