a review of the chemical ecology of antarctic marine invertebrates

AMER. ZOOL., 37:329-342 (1997)

A Review of the Chemical Ecology of Antarctic Marine Invertebrates1

JAMES B. MCCLINTOCK

Department of Biology, University of Alabama at Birmingham, Birmingham, Alabama

AND

BILL J. BAKER

Department of Chemistry, Florida Institute of Technology, Melbourne, Florida 32901

SYNOPSIS. The interdisciplinary field of marine invertebrate chemical ecology isrelatively young, and particularly so in polar marine environments. In this reviewwe present evidence that the incidence of chemical defense in antarctic benthicmarine invertebrate phyla is widespread. Mechanisms of chemical defense havebeen detected in antarctic representatives of the Porifera, Cnidaria, Brachiopoda,Tunicata, Nemertea, Mollusca and Echinodermata. This argues against earh'er bio-geographic theories that predicted a low incidence of chemical defense in polarwaters where levels of fish predation are low. Selection for chemical defense inbenthic sessile and sluggish marine invertebrates is likely a response to an envi-ronmentally stable community shown to be structured primarily by biotic factorssuch as predation and competition. Holoplankton and the eggs, embryos and larvaeof both benthic and planktonic antarctic macroinvertebrates may also employchemical defense to offset mortality during characteristically slow development andlong life span where susceptibility to predation is seemingly high. While most re-search to date has focused on the role of secondary metabolites in mediating pre-dation, it is likely that bioactive compounds in antarctic marine invertebrates alsoserve roles as antifoulants and allelochemics. The diversity of bioactive metabolitesdetected to date in antarctic marine invertebrates sets the stage both for continuingand for broadening efforts to evaluate their functional and ecological significance.

INTRODUCTION interactions and structuring marine com-The role of chemical defense in medial- munities (Bakus et al., 1986; Paul, 1992;

ing marine invertebrate predator-prey inter- Pawlik, 1993; Hay, 1996).actions has received considerable attention M o s t of the research on marine inverte-(reviewed by: Bakus et al., 1986; Paul, brate chemical ecology has focused on trop-1992; Pawlik, 1993; Hay, 1996). As is true ical environments (Bakus et al., 1986). Theof marine plants (Hay and Fenical, 1988; coral reefs of the tropics are well known forHay, 1992; Hay and Steinberg, 1992), ses- their high species diversity and communi-sile and sluggish marine invertebrates are ties comprised of individuals and coloniesextremely vulnerable to mobile predators, competing intensely for space and food.Moreover, marine invertebrates are subject Under such conditions, it is not surprisingto having their tissues fouled by settling lar- that many sessile or sluggish marine inver-vae, diatoms and other algal cells, and in tebrates have evolved chemical means ofthe case of sponges, soft corals, bryozoans defense (Bakus et al., 1986; Paul, 1992,and other sessile marine invertebrates, to Pawlik 1993; Faulkner, 1996 and referencesovergrowth by species competing for space, within). Early studies examining geograph-Ultimately, the ability of these organisms to j c patterns of chemical defense (as mea-chemically defend themselves can play a s u r e d b y ichthyotoxicity) in marine inver-significant role in regulating predator-prey tebrates noted a decrease in chemically de-

fended species as one moved from tropical1 invited mini-review. to temperate marine habitats (Bakus and

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330 J. B. MCCLINTOCK AND B. J. BAKER

Green, 1974; Green, 1977; Bakus, 1981).Based on these comparisons, and the ob-servation that fish predation on benthic ma-rine invertebrates decreased with increasinglatitude (Vermeij, 1978), an inverse corre-lation between chemical defense and lati-tude in marine invertebrates was proposed(Bakus and Green, 1974).

Although the antarctic benthic marine en-vironment has been classically consideredto be harsh environmentally, studies haveshown that with the exception of organismsliving in the most shallow water (less than33 m depth) where anchor ice and ice scourare important structuring forces (Dayton etal., 1969, 1970), the benthic community isremarkably rich and stable (Dell, 1972;Dayton et al., 1974; Richardson and Hedg-peth, 1977; Dayton 1989, 1990; White,1984). The assemblage of marine organ-isms comprising this community hasevolved during the events preceding thecretaceous breakup of Gondwanaland andthe movement of the antarctic continentsouthward. The establishment of a circum-polar current effectively isolated the conti-nent, and its climate remained temperate tosub-tropical until 22 million years ago(Dayton et al., 1994). The marine biota,therefore, has its origins in warmer climatesand is relatively old (Dell, 1972). Accord-ing to Dayton et al. (1994) the shallow-wa-ter antarctic marine fauna is derived from1) relict autochthonous fauna, 2) eurybathicfauna from deeper water, and 3) cool-tem-perate species, mostly from South America.

The factors responsible for structuringthis complex sponge-dominated communityappear to be primarily biological in nature.For example, competition for space is in-tense between certain species of sponges,several of which are capable of dominatingspace if released from predation pressure(Dayton et al., 1974; Dayton, 1989). More-over, although fish predators that browse onsessile marine invertebrates such as spongesare indeed rare in high latitudes (Eastman,1993), there is a very high incidence of pre-dation in Antarctica by mobile macroinver-tebrates, particularly echinoderms such assea stars (Dearborn, 1977; McClintock,1994). In the water column, there are a va-riety of abundant planktivorous fish that are

known to ingest zooplankton {e.g., Fosteret al., 1987; Eastman, 1991) as well as ex-tremely dense swarms of predatory amphi-pods {e.g., Rakusa-Suszczewski, 1972).While overall grazing or predation pressure(per unit time) is arguably higher in tropicalmarine systems (Vermeij, 1978), some an-tarctic macroinvertebrate grazers and pred-ators occur in extremely high densities andconsequently are capable of exerting con-siderable predation pressure (Fig. 1A).Moreover, antarctic organisms often havevery long lifespans (Clarke, 1983), the ef-fect of which may be that predation inten-sity averages out over lifespan to be similarto that in temperate or even tropical marinesystems (Fig. IB). As one of the oldest,most environmentally stable and intenselybiologically structured marine systems, theantarctic benthos is well suited for the evo-lution of chemical defense mechanisms.

There has been a plethora of bioactive sec-ondary metabolites (defined as those com-pounds with no definitive role in primarymetabolic pathways) isolated from marine in-vertebrates (Scheuer, 1990; Attaway and Za-borsky, 1993; Faulkner, 1996). These com-pounds have been isolated primarily fromsponges and cnidaria (predominantly soft cor-als), although smaller numbers of other mem-bers of marine invertebrate groups have alsoyielded bioactive secondary metabolites (Ba-ker, 1996; Faulkner, 1996 and referenceswithin). Although the descriptive chemicalstudies published on novel secondary metab-olites from marine invertebrates number inthe thousands, there are comparatively fewstudies which provide ecological informationabout the functional significance of thesecompounds. In many instances, biological ac-tivity has been measured simply as the abilityof a compound to cause cell lysis or inhibitgrowth of a non-marine microbe. While suchinformation may have utility in pharmaceu-tical studies (Munro et al., 1987; Scheuer,1990; Hay and Fenical, 1996), much remainsto be learned about the ecological signifi-cance of such bioactive compounds. This isparticularly true in polar waters, where chem-ical ecological studies of marine invertebrateshave only recently begun, with the vast ma-jority of studies having been conducted inMcMurdo Sound, Antarctica (77°S, 166°E).

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CHEMICAL ECOLOGY OF ANTARCTIC MARINE INVERTEBRATES 331

FIG. 1. In situ photographs of antarctic benthic predation events representative of different time scales. A. Massfeeding aggregation of the antarctic nemertean worm Parborlasia corrugatus and the antarctic sea star Odontastervalidus. These common predation events may occur over a time scale of a few hours (McClintock, Baker, Heine pers.obs.; photo by J. Heine). B. The antarctic spongivorous sea star Acodontaster conspicuus preying on a large vasesponge. These predation events may last months to years (Dayton et al., 1974; photo by J. Mastro).

While the data base for antarctic waters isconsequently regional in its scope, it can beexpected to have wide applicability as theshallow epi-macrofauna of McMurdo Soundis generally circumpolar in its distribution(Hedgpeth, 1969; Dell, 1972; Arnaud, 1974;White, 1984). The purpose of this paper is toprovide an overview of what is currentlyknown of the chemical ecology of antarcticmarine invertebrates and suggest directionsfor further research. We include in this reviewboth information on the broad bioactive na-ture of secondary metabolites and whereverpossible information that is of ecological sig-nificance. To date, ecological studies in Ant-arctica have focused primarily on evaluationsof how defensive chemistry may inhibit feed-ing by likely or known predators, similar tostudies in temperate and tropical marine en-vironments (Paul, 1992; Pawlik, 1993; Hay,1996).

EMPIRICAL STUDIES

Sessile macroinvertebratesSponges.—The sponges of McMurdo

Sound, Antarctica have been the focus ofchemical studies to date (Table 1). On the

eastern side of McMurdo Sound, Antarcti-ca, approximately twenty-one species ofconspicuous marine sponges occur in near-shore waters accounting for 55% of thebenthic surface area below 33 m depth(Koltun, 1970; Dayton et al., 1974). Dayton{et al., 1974) was the first to suggest chem-ical defenses occurred in antarctic sponges,having observed no predation on the spong-es Leucetta leptorhapsis, Dendrilla mem-branosa and Isodictya erinacea, all ofwhich apparently lacked physical defensesagainst spongivorous sea stars. In the firstquantitative studies of chemical bioactivity,McClintock (1987) and McClintock andGauthier (1992) found a number of antarc-tic sponge extracts caused mortality ingoldfish or inhibited growth in allopatricmicroorganisms. Moreover, Blunt et al.(1990) found the incidence of antiviral ac-tivity similar in marine sponges from tem-perate waters of New Zealand (37%) andpolar antarctic waters (33%). In addition,Battershill (1990) conducted immunologi-cal assays with three antarctic sponges fromMcMurdo Sound (Cinachyra antartica, La-trunculia sp., Polymastia sp.) and found

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TABLE 1. Chemical and ecological bioactivirf of antarctic shallow-water marine invertebrate.

PORIFERACalyx acuariusCinachyra antarcticaDendrilla membranosaGellius benedeniHaliclona sp.Haliclona dancoiHomaxonella balfourensisInflatella bellilsodictya erinaceaKirkpatrickia variolosaLatrunculia apicalisLeucetta leptorhapsisPolymastia invaginataRosella nudaRosella racovitzaeSphaerotylus antarcticusTetilla leptoderma

Tube-foot Feeding

retrac- deter- Activity in:

mirnL fntt. Pyln. t~nm- Whrtlf

bial lant toxic Sea stars Fish pound Extract Tissue animal Reference11

+ + + 1+ + 1,2,3,4,5,6

+ + + + 1,2+ + + 1,2

+ + 1+ + + 1,2+ + + ,2

+ + 1+ + + + +' 1,2,3+ + + + 1,2,3,7,8,9+ + + + ,2,3,6,10+ + + + + 1,2,3+ + + 1,2

+ + 1+ + 1+ + 1+ + 1

CNIDARIAAlcyonium paessleriClavularia franklinianaGersemia antarctica

BRACHIOPODALiothyrella uvaASCIDACEACnemidocarpa verrucosaNEMERTEAParborlasia corrugatusMOLLUSCAAustrodoris kerguelensisClione antarcticaMarseniopsis mollisTritoniella belli

ECHINODERMATAPerknaster fuscusDiplasterias brucei

11,12,1311,12,1311,12,13

14

15

16,17

18,19,202,21,22,2318,19,2418,19,25

2627

0 Data only presented for species tested against antarctic microbes, microalgae, macroinvertebrate gametes,macroinvertebrates or fish.

"References: McClintock et at, 1993a1; Baker and McClintock unpublished2; Baker et al., 19933, 1995";Molinski and Faulkner, 19875; Yang et al, 19956; Jayatilake et al., 19957; Perry et al., 19948; Trimurtulu et al.,19949; Blunt et al, 1990'°; Slattery and McClintock, 1995"; Slattery et al, 199512; Slattery, 1994'3; McClintocketal, 1993fc14; McClintock et al, 199115; Heine et al., 199116; W. Kem unpublished17; McClintock et al, 1992a18;McClintock et al, 1994d19; Davies-Coleman and Faulkner, 199120; McClintock and Janssen, 199021; Bryan etal, 199522; Yoshida et al, 199523; McClintock et al, 199424; McClintock el al, 1994c25; McClintock et al,1992£26; McClintock and Baker, 199727.

c Whole animal activity detected in developing embryos.

them all capable of rejecting tissues fromcongeners, concluding these sponges werecapable of producing defensive chemicalsthat were toxic to genetically dissimilar tis-

sues. The results of these studies suggestedthat a variety of antarctic sponges harbortoxic compounds. Nonetheless, while thesebioassay approaches provide useful infor-

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Dendrillin

?H

Discorhabdin G

Eribusenone

Variolin A

FIG. 2. Chemical structures of bioactive compounds isolated from antarctic organisms (clockwise from upperleft): The bacterium Pseudomonas aeruginosa isolated from the surface of the sponge Isodictya setifera, thepteropod Clione antarctica, and the sponges Isodictya erinacea, Dendrilla membranosa, Latrunculia apicalisand Kirkpatrickia variolosa.

mation which may be of pharmacologicalor agrochemical importance, they providelittle information of demonstrative ecolog-ical significance. Subsequent investigationsby McClintock et al. (1994a) focused onexaminations of the feeding deterrent char-acteristics of hexane, chloroform and meth-anol (non-polar to polar) extracts of antarc-tic sponges employing a tube-foot assay us-ing an ecologically relevant predator, thecommon antarctic spongivorous sea starPerknaster fuscus. Significant tube-foot re-traction activity was detected in the chlo-roform and methanol extracts of 75% ofeighteen species tested. These levels of de-terrence are similar to levels measured inreef fish presented feeding pellets contain-ing extracts of Caribbean sponges in thelaboratory (Pawlik et al., 1995). The bioac-tive compounds likely responsible for feed-ing deterrence or additional biological ac-tivity have been elucidated in five of theseantarctic species.

A variety of bioactive metabolites havebeen identified from antarctic sponges (Ba-ker et al., 1993, 1994; Fig. 2). Diterpenemetabolites, including dendrillin, 9,11-di-hydrogracilin A, membranolide and picol-inic acid have been extracted from the tis-sues of Dendrilla membranosa (Molinskiand Faulkner, 1987, 1988; Baker et al.,1993, 1994, 1995). The latter compoundcauses sea star tube-foot retraction (Mc-

Clintock et al., \994b). Kirkpatrickia vari-olosa has been found to produce variolins,a novel group of alkaloids, which have beendemonstrated to have antitumor and anti-viral activity (Perry et al., 1994; Trimurtuluet al., 1994). A purple pigment in K. vari-olosa causes tube-foot retraction in the an-tarctic sea star Perknaster fuscus (Bakerand McClintock, unpublished). Moreover, abioactive stilbene derivative has been iso-lated from K. variolosa, the first such ob-servation of a stilbene from a marine in-vertebrate (Jayatilake et al., 1995). The an-tarctic sponge Latrunculia apicalis has beenfound to contain a variety of discorhabdinpigments (Yang et al., 1995; Baker et al.,1993, 1994) which are cytotoxic (Blunt etal., 1990) and cause tube-foot retraction inP. fuscus (Baker and McClintock, unpub-lished). Recent work with the sponge Leu-cetta leptorhapsis has indicated the pres-ence of highly cytotoxic lipids (Baker et al.,1993) that cause feeding deterrence in an-tarctic seastars (McClintock et al., 1993a).The antarctic sponge Isodictya erinaceacontains the secondary metabolites eribu-senone, 7-methyladinine, and p-hydroxy-benzoic acid (Baker et al., 1994; Moon etal., in preparation). Bioactive metaboliteshave also been isolated from microbes as-sociated with antarctic sponges. Jayatilakeet al. (1996) recently isolated a series ofdiketopiperazines and phenazine alkaloids

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from the bacterium Pseudomonas aerugi-nosa associated with the antarctic spongeIsodictya setifera (Fig 2.)- Finally, the an-tarctic sponge Artemisina apollinis has beenfound to possess 28 steroidal derivatives in-cluding a new group of natural products(Seldes et al, 1990). The ecological rolesof bioactive compounds isolated from L.leptorhapsis, I. erinacea, and /. setifera arecurrently unknown.

Although it is possible that some of thebioactive metabolites in antarctic spongesare "evolutionary baggage" with no cur-rent adaptive significance, it is more likelythat given the extreme age of the marinebenthos, there has been ample time for de-fensive metabolites to have evolved in re-sponse to sympatric predators, fouling or-ganisms, or competitors. In this respect, itis of interest to consider whether congenersfrom other latitudes have similar or differ-ent chemical defenses, or lack chemical de-fenses entirely. The answer appears to varywith species, as might be expected ofsponges under different selective pressures.For example, the antarctic congeners ofHaliclona and Mycale are devoid of thetypes of secondary metabolites found intheir tropical counterparts (alkaloids in Hal-iclona (Schmitz et al., 1978; Sakai et al.,1986; Baker et al., 1988; Crews et al.,1994) and terpenes or mycalamides fromMycale (Perry et al., 1988; Fusetani et al.,1991; Tanaka et al., 1993)). Alternately, an-tarctic Latrunculia and Dendrilla both pro-duce derivatives (discorhabdin G and den-drillin, respectively [Yang et al., 1995; Ba-ker et al., 1995]) of secondary metabolitesfound in temperate and tropical congeners(Karuso et al, 1984; Mayol et al, 1985;Molinski and Faulkner, 1987; Blunt et al,1990) and the tropical sponge Leucetta mi-croraphis harbors leucettamols (Kong andFaulkner, 1993) that are similar in structureto cytotoxic lipids produced by the antarcticcongener Leucetta leptorhapsis (Baker etal., 1993). More information is needed toprovide a more comprehensive evaluationof phylogenetic influences on patterns ofchemical defense in antarctic sponges.

In many cases it is those antarctic spong-es with color that have proven to be bioac-tive to date (Baker and McClintock, per-

sonal observation). At first examinationthese would appear to be examples of warn-ing coloration or aposematism (Guilfordand Cuthill, 1991; Rosenberg, 1991). How-ever, Pawlik et al. (1995) found no evi-dence of aposematism in tropical marinesponges. Moreover, it is unlikely aposema-tism occurs in antarctic sponges, as the an-tarctic marine benthos is depauperate in vi-sually oriented browsing predators such asfish which feed on sessile invertebrates(most antarctic benthic fish eat crustaceans;Eastman, 1991, 1993). In this regard, evenif aposematism occurred in sponges (butsee Pawlik et al, 1995), there should belittle evolutionary selection for warningcoloration in antarctic sponges when theirprimary predators are sea stars (Dearborn,1977; McClintock, 1994), which orient toprey chemically (Sloan, 1980). Nonethe-less, it is intriguing that antarctic spongesemploy their colored pigments as a chemi-cal defense. For example, pigments fromthe colored sponges Latrunculia apicalisand Kirkpatrickia variolosa are bioactiveand cause sea star tube-foot retraction (Ba-ker and McClintock, unpublished).

Soft corals.—Chemical studies of antarc-tic soft corals have focused on three antarc-tic species that occur in McMurdo Sound(Table 1). Two of these species, Alcyoniumpaessleri and Clavularia frankliniana areextremely abundant along the east side ofMcMurdo Sound (Dayton et al, 1974; Slat-tery, 1994). The third species, Gersemiaantarctica, is much rarer, and within Mc-Murdo Sound is confined to its westernregions (Slattery and McClintock, 1995).All three of these soft corals are chemicallydefended. Organic extracts of A. paessleriand G. antarctica inhibit the attachment ofmarine antarctic bacteria (Slattery et al,1995). In addition, organic extracts exhibitantifoulant activity in field experimentscausing inhibition of diatom settlement.This is important as diatoms are one of theprimary fouling organisms in antarctic ben-thos (El-Sayed and Fryxell, 1993). Two po-tential soft coral predators, the antarctic seastars Odontaster validus and Perknasterfuscus, show tube-foot retractions to organ-ic and aqueous extracts of all three soft cor-al species (Slattery and McClintock, 1995).

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Aqueous homogenates of two of the softcorals, A. paessleri and G. antarctica, aretoxic to antarctic sea urchin larvae, sug-gesting that similar to tropical marine in-vertebrates toxicity and feeding deterrenceare not predictably related (Pawlik et al.,1995). Distinct secondary metabolites re-sponsible for toxicity or feeding deterrencemay be present in these soft corals (Slatteryet al., 1995). Chimyl alcohol has been de-tected in the tissues of C. frankliniana andcauses rejection of treated shrimp-discs inthe omnivorous sea star Odontaster validus(McClintock et al., 1994c).

Bryozoans.—While antarctic bryozoanscan be dominant members of antarctic ben-thic communities (Foster, 1969), only onestudy has investigated their biological activ-ity. Winston and Bemheimer (1986) inves-tigated the extracts of five species of an-tarctic bryozoans collected from the Ant-arctic Peninsula and examined hemolyticactivity against mammalian erythrocytes.Extracts of one species, Carbasea curva,caused significant lysis of mammalian cells,suggesting the presence of bioactive sec-ondary metabolites. No investigations haveyet been conducted to determine the natureof the secondary metabolite(s) nor to ex-amine their ecological significance. Win-ston and Bernheimer (1986) indicate that C.curva is one of the most abundant bryozo-ans found in benthic samples from the Ant-arctic Peninsula or the Ross Sea, and thatthe toxic substance may be employed inchemical defense, explaining the success ofa weakly calcified body plan.

Brachiopods.—One of the few AntarcticPeninsular organisms which has been stud-ied for its chemical defense is the commonantarctic brachiopod Liothyrella uva. Thispunctate terebratulid species is common atdepths of 5-300 m (Voss, 1988). Ecologicalassays indicate that extracts of whole softbody tissues cause significant retraction ofthe sensory tube-feet of six species of an-tarctic sea stars (Table 1; McClintock et al.,19936), several of which are likely preda-tors of brachiopods (McClintock, 1994).Ground body tissues embedded in agar pel-lets containing krill meal resulted in signif-icant feeding deterrence in an allopatricfish, the Sheepshead Minnow Cyprinidon

variegatus (McClintock et al., 19936).Studies are needed to determine if ecolog-ically relevant fish are also deterred. Thenature of the bioactive compound(s) re-sponsible for feeding deterrence are un-known. The results of this study furthersupport the hypothesis that unpalatabilityoccurs in brachiopods in temperate, tropi-cal, and polar environments (Thayer andAllmon, 1991). A chemical means of de-fense may be particularly important from anevolutionary perspective due to the slowgrowth and late reproduction which char-acterizes the life history of brachiopods(Thayer, 1985).

Ascidians.—Although there are manyspecies of antarctic ascidians, only one spe-cies has been chemically investigated. Thecommon solitary ascidian Cnemidocarpaverrucosa is a large conspicuous specieswhich is found in McMurdo Sound, and hasa circumpolar distribution (Kott, 1969;Dayton et al., 1974). McClintock et al.(1991) conducted an analysis of the palat-ability and chemical defense of the tunic,ovitestes, branchial basket, body wall, en-docarps and intestines. They found that thetunic was deterrent to sympatric pelagic andbenthic fish, in addition to an allopatric fishmodel (Table 1). Nonetheless, homogenatesof the tunic were not cytotoxic to sea urchingametes, suggesting that the bioactive com-pound^) are not toxic. The heavy foulingof the tunic surface by bryozoans and hy-droids indicates that bioactive chemicals arenot effective antifoulants. Mature ovitestesare rejected by antarctic fish and alginatekrill pellets containing lipophilic extracts ofovitestes are rejected by the antarctic seastar Odontaster validus, a likely predator ofsettling larvae (Dayton et al., 1974), indi-cating that the eggs and larvae may possessa chemical defense (McClintock et al.,1991; McClintock and Baker, unpublished).

Mobile macroinvertebratesNemerteans.—One of the most conspic-

uous benthic invertebrates in shallow an-tarctic waters is the large (up to 1 m ex-tended body length) nemertean worm Par-borlasia corrugatus (Fig. 1A; Knox, 1970,Gibson, 1983). Despite their high abun-dance and rich energy content, and obvious

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lack of skeletal defenses, individuals arerarely if ever preyed upon (Dayton et al.,1974; Heine et al, 1991). Cytotoxicity as-says indicate homogenates of the wholebody tissues cause mortality in gametes ofthe antarctic sea urchin Sterechinus neu-mayeri. In addition, ecological bioassays in-dicate two common species of antarctic fishshow significant rejection of body tissues(Table 1; Heine et al, 1991). Both toxicityand feeding-deterrent characteristics of thisspecies may result from the production ofa copious acidic (pH = 3.5) mucus (Heineet al., 1991). The defensive properties ofthis acidic mucus may be diminishedthrough neutralization in seawater. None-theless, the mucus of P. corrugatus alsoharbors a potent toxic neuropeptide (Wil-liam Kem, unpublished).

Molluscs.—Investigations of chemical de-fense in antarctic molluscs have been limitedto species occurring in McMurdo Sound (Ta-ble 1). Nonetheless, many of these specieshave circumpolar distributions, and their de-fensive chemistry is likely similar across awide geographic range. Ecological bioassaysindicate the mantle tissues of the antarctic nu-dibranchs Austrodoris kerguelensis and Tri-toniella belli are rejected by two species ofsympatric antarctic fish, and cause significanttube-foot retractions in four species of sym-patric antarctic sea stars (McClintock et al,1992a). Austrodoris kerguelensis produces aseries of bioactive acid glycerides (Davies-Coleman and Faulkner, 1991) which remainto be evaluated for ecological function, whileT. belli contains chimyl alcohol which causesfeeding deterrence in the sea star Odontastervalidus (McClintock et al, 1994b). Thisproven feeding deterrent may be derivedfrom its diet of the soft coral Clavulariafrankliniana (McClintock et al, 19946). Theprosobranch Marseniopsis mollis, which hasan internalized vestigial shell, has mantle tis-sues which are rejected by antarctic fish andsea stars (McClintock et al, 1992a) and thecompound homarine has been isolated fromthe mantle, foot and viscera (McClintock etal., 1994c). Homarine causes feeding deter-rence in the omnivorous O. validus at levelsspanning those detected in the body tissuesof M. mollis (McClintock et al, 1994c).Homarine was not found in the tunic of the

antarctic ascidian Cnemidocarpa verrucosa,the presumed primary prey of this gastropod(McClintock et al., 1994c). Nonetheless,homarine has been isolated from the denseassemblage of epizooites which foul the tunicof this ascidian (McClintock et al, 1994c),suggesting that these fouling organisms (pri-marily bryozoans and hydroids) may begrazed by M. mollis and be the dietary sourceof this defensive compound.

The common pelagic pteropod Clioneantarctica occurs in vast swarms seasonallyin antarctic continental shelf waters (Foster,1987). Intact live sea butterflies and wholebody homogenates imbedded in pellets con-taining feeding stimulants are consistentlyrejected by the antarctic zooplanktivorousfish Pagothenia borchgrevinki, a significantpteropod predator (Foster et al, 1987), in-dicating the presence of chemical defense(McClintock and Janssen, 1990). Interest-ingly, the abundant antarctic hyperiid am-phipod Hyperiella dilatata abducts and car-ries a single live individual of C. antarctica(Fig. 3), providing itself with a means ofchemical defense from fish predators(McClintock and Janssen, 1990). The na-ture of the compound responsible for chem-ical deterrence in C. antarctica has recentlybeen elucidated to be a novel bioactive lin-ear hydroxyketone, named pteroenone (Fig.2; Bryan et al, 1995; Yoshida et al, 1995).This is one of the first defensive compoundsisolated from a planktonic macroinverte-brate, and supports recent evidence thatfeeding deterrent properties of oceanic hol-oplankton may be widespread (McClintocket al., 1996). As C. antarctica is extremelyabundant, the trophic implications of chem-ical defense in modeling energy flow in theantarctic water column must be considered.Moreover, if additional organisms receivedefensive characteristics through their as-sociation with chemically defended species(e.g., McClintock and Jansson, 1990), thisfurthers the complexity of planktonic eco-systems (McClintock et al, 1996).

Echinoderms.—Research conducted withtemperate and tropical echinoderms has in-dicated that a large number of species maypossess bioactive compounds, particularlythose which are saponin-related (Verbist,1993). Bioactivity appears to occur most fre-

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FIG. 3. The antarctic hyperiid amphipod Hyperiella dilatata shown grasping the chemically defended pteropodCtione antarctica (McClintock and Janssen, 1990). This unique association provides a mechanism for amphipodsto defend themselves against their primary predators, antarctic fish. Magnification is approximately X500.

quently in the body tissues of the holothuri-ans and asteroids (Mackie et ai, 1977).McClintock (1989) examined the toxicity ofthe body wall of 23 species of antarctic echi-noderms to the mosquitofish Gambusia a/fin-is. Patterns of toxicity were class specific, andsimilar to patterns seen in temperate and trop-ical species, with the highest levels of toxicityoccurring in the body tissues of holothuroidsand asteroids. Two of three species of holo-thuroids tested were toxic, while seven ofthirteen species of asteroids tested causedmortality in fish. Toxicity was not found tobe related to the amount of skeletal materialpresent in the echinoderm body wall, al-though the degree of skeletal armament wasgenerally low among antarctic species(McClintock, 1989).

The common spongivorous sea star Perk-naster fuscus possesses the bioactive tetra-hydroisoquinoline alkaloid fuscusine (Konget ai, 1992). This is only the second reportof an alkaloid in the body wall tissues of a

sea star, the first being imbricatine, a ben-zyltetrahydroisoquinoline alkaloid whichoccurs in the sea star Dermasterias imbri-cata on the west coast of North America.This compound is known to induce a flightresponse in a sea anemone (Patherina andAnderson, 1986). Crude homogenates ofthe body wall tissues of P. fuscus are toxicto the sperm of the antarctic sea urchinSterechinus neumayeri, cause an inhibitionof the righting response of the antarctic seastar Odontaster validus, and elicit signifi-cant tube-foot retractions in the sympatricantarctic sea stars O. validus, O. meridion-alis, Acodontaster conspicuus and Diplas-terias brucei (Table 1; McClintock et al.,\992b). At least one of these sea stars,Odontaster validus, is an opportunisticechinovore (McClintock, 1994). It is ofsome significance that while a number ofantarctic sea stars are included in the dietsof echinoderms and sea anemones (Dear-born, 1977), P. fuscus has never been ob-

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served as a prey item (Dayton et al., 1974).This may be attributable to its chemical de-fense! Possessing such an effective meansof defense has important ramifications inmaintaining populations of this spongivo-rous sea star, as it is responsible for keepingone of the primary space-dominating an-tarctic sponges (Mycale acerata) at levelswhich allow increased species diversity(Dayton et al., 1974). Steroidal glycosidesand polyhydroxylated steroids have recent-ly been isolated from the antarctic sea starAcodontaster conspicuus and the ophiu-roids Ophiosparta gigas and Ophionotusvictoriae (D'Auria et al., 1993, 1995; loriz-zi et al., 1996; De Marino et al., 1997).Bioassays indicate that steroidal glycosidesand polyhydroxylated steroids isolated fromA. conspicuus cause significant growth in-hibition in three species of antarctic marinebacteria isolated from the surfaces of an-tarctic sponges and echinoderms (De Ma-rino et al., in press). This suggests one eco-logical role of these compounds may be inthe prevention of microbial fouling.

In one of only two studies to focus on thechemical defense of early life stages of an-tarctic marine invertebrates, McClintock andVernon (1990) examined the icthyonoxiccharacteristics of the eggs and embryos offifteen species of antarctic echinoderms, pri-marily sea stars. Using the common killifishFundulus grandis as a model predator, theyoffered pellets impregnated with echinodermtissues and a feeding stimulant to fish. Chem-ical feeding deterrents occurred in the largeyolky eggs of the pelagic lecithotrophic seastars Perknaster fuscus and Porania antarc-tica. Brooded embryos of the sea stars No-tasterias armata and Diplasterias bruceiwere also noxious. The chemical deterrentswere effective at ecologically relevant con-centrations. In a more recent study, Mc-Clintock and Baker (1997) demonstrated thatthe lecithotrophic eggs, embryos and larvaeof five species of antarctic marine inverte-brates (including three echinoderms) wereunpalatable or chemically defended from eco-logically relevant benthic and water columninvertebrate predators (sea stars, sea anemo-nes and amphipods). Two echinoderms withplanktotrophic modes of reproduction (thesea urchin Sterediinus neiimayeri and the sea

star Odontaster validus) lacked chemical de-fense in their eggs or larvae. Therefore, sim-ilar to tropical marine invertebrates (Lindqu-ist and Hay, 1996), large yolky lecithotrophicembryos and larvae are more likely to bechemically defended. This may be especiallytrue in antarctic embryos or larvae wherevery slow development results in substantialperiods of time spent in the plankton or onthe benthos (Pearse et al., 1991).

SUMMARY AND FUTURE DIRECTIONS

The unique environmental and biotic fac-tors that characterize shallow antarctic shelfwaters have resulted in communities struc-tured by biotic factors such as predation andcompetition (Dayton et al., 1974). The pres-ent review indicates that selection for eco-logically relevant secondary metaboliteshas occurred in a wide variety of represen-tative organisms (reviewed in Table 1).Nonetheless, while much of the researchconducted to date on chemical defense hasbeen conducted in the laboratory using eco-logically relevant predators (as essentiallyhas been the case for temperate and tropicalmarine invertebrates), there is a need to ex-tend studies to the field, as has been doneto a limited extent in tropical marine envi-ronments (Paul, 1992; Pawlik, 1993; Hay,1996). Much also remains to be learnedabout additional novel bioactive com-pounds, and there is a need for further eval-uation of the functional roles of knowncompounds. In addition to defense frompredation, factors most likely to be medi-ated by defensive metabolites include foul-ing and allelochemical interactions. For ex-ample, sessile antarctic benthic organismsare subject to particularly intense foulingpressure by benthic diatoms. Allelochem-istry could be important because in contrastto the generalized perception of reducedgrowth rates in polar species, there are spe-cies that grow rapidly and crowd out otherspecies, eventually monopolizing space ifreleased from predation (Dayton et al.,1974, Dayton, 1989).

To date, few investigations have extend-ed studies of defensive metabolites to an-tarctic macroalgae (Amsler et al., submit-ted). Such studies will be of particular in-terest given current theories relating defen-

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sive chemistry in macroalgae tobiogeographic patterns of herbivory (Estesand Steinberg, 1988; Steinberg and Paul,1990; Hay, 1992). Initial investigation sug-gests that antarctic brown algae produce de-fensive polyphenolics, similar to their tem-perate and tropical counterparts, perhapsexplaining their seemingly low levels ofherbivory (Amsler, McClintock and Baker,unpublished).

As in all planktonic systems, there is aneed to extend the evaluation of chemicaldefense to marine invertebrate holoplank-tonic organisms in antarctic waters. Of par-ticular interest will be those holoplanktonicorganisms that comprise significant bio-mass in pelagic foodwebs, such as salps andpteropods. Chemically mediated predationmay have profound effects on modeling en-ergy flow in such systems (McClintock etal., 1996). Moreover, more information onthe role of secondary metabolites in medi-ating patterns of predation on the pelagicembryos and larvae of macroinvertebratesis needed, along with more quantitative in-formation on abundances and diets of likelyplanktonic predators.

Finally, studies are needed to determine ifantarctic microorganisms (e.g., bacteria, mi-croalgae) employ defensive chemistry (e.g.,Jayatilake et al., 1996), if macroinvertebratesutilize microbial defensive metabolites, and ifdefensive chemistry in antarctic organisms isstatic or can be induced in response to a va-riety of ecological constraints.

ACKNOWLEDGMENTS

We would like to acknowledge the Nation-al Science Foundation, the Antarctic SupportAssociates Inc., and the US Naval AntarcticSupport Force for their generous support ofour antarctic research program (JBM: NSFGrant numbers OPP-8815959, OPP-9118864,OPP-9530735; BJB: NSF Grant numbersOPP-9117216, OPP-9526610). This paperwas also supported in part by the Universityof Alabama at Birmingham Caroline P. andCharles W. Ireland Award for Scholarly Dis-tinction to JBM. Dr. Polly Penhale, ProgramManager of the Office of Polar Programs atNSF, has been particularly helpful. Much ofthe research reviewed in the present paperwould not have been possible without the

outstanding efforts of our Research Col-leagues, Postdoctoral Fellows, Graduate Stu-dents, Technicians and Research Divers.These include C. Amsler, J. Baker, S. Bowser,P. Bryan, D. Coleman, P. Dayton, A. DeVries,J. Faulkner, J. Gauthier, J. Grimwade, M. Ha-mann, G. Hines, J. Janssen, G. Jayatilake, R.Kopitzke, T. Klinger, J. Kreider, J. Lawrence,A. Leonard, J. Mastro, C. Moeller, B. Moon,A. San-Martin, C. Thayer, M. Thornton, EScheuer, G. Schinner, M. Slattery, D. Tedes-chi, J. Vernon, S. Watts, A. Yang, and W.Yoshida. The paper benefited from the help-ful comments of C. Amsler, G. Jayatilake, A.Marsh and J. Pawlik. We wish to dedicatethis paper to Feme McClintock and Jill Ba-ker.

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