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Biochemical composition, energy content and chemical antifeedant and antifoulant defenses of the colonial Antarctic ascidian Distaplia cylindrica

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Abstract

The colonial ascidian Distaplia cylindrica occurs both as scattered individual colonies or in “gardens” of colonies in fine-grained soft substrata below 20 m depths off Anvers Island along the Antarctic Peninsula. Individual colonies, shaped as tall rod-like cylinders and anchored in the sediments by a bulbous base, may measure up to 7 m in height. D. cylindrica represent a considerable source of materials and energy for prospective predators, as well as potential surface area for fouling organisms. Nonetheless, qualitative in situ observations provided no evidence of predation by sympatric predators such as abundant sea stars, nor obvious biofouling of colony surfaces. Mean energy content of whole-colony tissue of D. cylindrica was relatively high for an ascidian (14.7 kJ g−1 dry wt), with most of this energy attributable to protein (12.7 kJ g−1 dry wt). The sympatric omnivorous sea star Odontaster validus consistently rejected pieces of D. cylindrica colonies in laboratory feeding assays, while readily ingesting similarly sized alginate food pellets. Feeding deterrence was determined to be attributable to defensive chemistry, as colonies of D. cylindrica are nutritionally attractive and lack physical protection (conspicuous skeletal elements or a tough outer tunic), and O. validus display significant feeding-deterrent responses to alginate food pellets containing tissue-level concentrations of organic extracts. In addition, high acidity measured on outer colony surfaces (pH 1.5) as well as homogenized whole-colony tissues (pH 2.5) are indicative of surface sequestration of inorganic acids. Agar food pellets prepared at tissue levels of acidity resulted in significant feeding deterrence in sea stars. Thus, both inorganic acids and secondary metabolites contribute to chemical feeding defenses. D. cylindrica also possesses potent antifoulant secondary metabolites. Tissue-level concentrations of hydrophilic and lipophilic extracts caused significant mortality in a sympatric pennate diatom. Chemical feeding deterrents and antifoulants are likely to contribute to the abundance of D. cylindrica and, in turn, play a role in regulating energy transfer and community structure in benthic marine environments surrounding Antarctica.

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References

  • Amsler CD, McClintock JB, Baker BJ (2000a) Chemical defenses of Antarctic marine organisms: a re-evaluation of the latitudinal hypothesis. In: Davison W, Howard-Williams C, Broadey P (eds) Antarctic ecosystems: models for wider ecological understanding. Proceedings of the 7th SCAR international biology symposium. N.Z. Natural Science, Christchurch, New Zealand, pp 158–164

  • Amsler CD, Moeller CB, McClintock JB, Iken KB, Baker BJ (2000b) Chemical defenses against diatom fouling in Antarctic marine sponges. Biofouling 16:29–45

    CAS  Google Scholar 

  • Amsler CD, Iken KB, McClintock JB, Baker BJ (2001a) Secondary metabolites from antarctic marine organisms and their ecological implications. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, Fla., pp 267–300

  • Amsler CD, McClintock JB, Baker BJ (2001b) Secondary metabolites as mediators of trophic interactions among antarctic marine organisms. Am Zool 41:17–26

    CAS  Google Scholar 

  • Arntz WE, Gutt J, Klages M (1997) Antarctic marine biodiversity: In: Battaglia B, Valenica J, Walton DWH (eds) Antarctic communities: species, structure and survival. Cambridge University Press, Cambridge, pp 3–14

  • Bakus GJ (1981) Chemical defense mechanisms of the Great Barrier Reef, Australia. Science 211:497–498

    CAS  PubMed  Google Scholar 

  • Bakus GJ, Green G (1974) Toxicity of sponges and holothurians: a geographic pattern. Science 185:951–953

    Google Scholar 

  • Bavestrello G, Arillo A, Calcinai C, Lanza S, Ara M, Cattaneo-Vietti R, Gaino E (2000) Parasitic diatoms inside Antarctic sponges. Biol Bull (Woods Hole) 198:29–33

    Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein using the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brey T, Rumohr H, Ankar S (1988) Energy content of macrobenthic invertebrates: general conversion factors from weight to energy. J Exp Mar Biol Ecol 117:271–278

    Article  Google Scholar 

  • Brody S (1945) Bioenergetics and growth. Hafner, New York

  • Bryan PJ, McClintock JB, Slattery M, Rittschof DP (2003) A comparative study of the non-acidic chemically mediated antifoulant properties of three sympatric species of ascidians associated with seagrass habitats. Biofouling 18:235–245

    Article  Google Scholar 

  • Cerrano C, Arillo A, Bavestrello G, Calcinai B, Cattaneo-Vietti R, Penna A, Sara M, Totti C (2000) Diatom invasion in the antarctic hexactinellid sponge Scolymastia joubini. Polar Biol 23:441–444

    Article  Google Scholar 

  • Chanas B, Pawlik JR (1995) Defenses of Caribbean sponges against predatory reef fish. II. Spicules, tissue toughness, and nutritional quality. Mar Ecol Prog Ser 127:195–211

    Google Scholar 

  • Chanas B, Pawlik JR (1996) Does the skeleton of a sponge provide a defense against predatory reef fish? Oecologia 107:225–231

    Google Scholar 

  • Cronin G (2001) Resource allocation in seaweeds and marine invertebrates: chemical defense patterns in relation to defense theories. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, Fla., pp 325–354

  • Davis AR (1991) Alkaloids and ascidian chemical defense: evidence for the ecological role of natural products from Eudistoma olivaceum. Mar Biol 111:375–379

    Google Scholar 

  • Davis AR, Wright AE (1989) Interspecific differences in fouling of two congeneric ascidians (Eudistoma olivaceum and E. capsulatum): is surface acidity an effective defense? Mar Biol 102:491–497

    Google Scholar 

  • Dayton PK, Robilliard GA, DeVries AL (1969) Anchor ice formation in McMurdo Sound, Antarctica and its biological effects. Science 163:273–274

    Google Scholar 

  • Dayton PK, Robilliard GA, Paine RT, Dayton LB (1974) Biological accommodation in the benthic community at McMurdo Sound, Antarctica. Ecol Monogr 44:105–128

    Google Scholar 

  • Dayton PK, Mordida BJ, Bacon F (1994) Polar marine communities. Am Zool 34:90–100

    Google Scholar 

  • Dearborn JH (1977) Foods and feeding characteristics of antarctic asteroids and ophioroids. In: Llano GA (ed) Adaptations with antarctic ecosystems. Smithsonian Institution, Washington DC, pp 293–326

  • Dell RK (1972) Antarctic benthos. Adv Mar Biol 10:1–216

    Google Scholar 

  • Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith R (1953) Colorimetric determination of sugars and related substances. Anal Chem 28:350–356

    Google Scholar 

  • Eastman J (1994) Antarctic fish biology. Academic, San Diego

  • Faulkner DJ (2000) Marine natural products. Nat Prod Rep 1:7–55

    Article  Google Scholar 

  • Freeman NK, Lindgren FT, Ng YC, Nichols AV (1957) Infrared spectra of some lipoproteins and related lipids. J Biol Chem 203:293–304

    Google Scholar 

  • Furrow FB, Amlser CD, McClintock JB, Baker BJ (2003) Surface sequestration of chemical feeding deterrents in the Antarctic sponge Latrunculia apicalis as an optimal defense against sea star spongivory. Mar Biol 143:443–449

    Article  Google Scholar 

  • Green G (1977) Ecology of toxicity in marine sponges. Mar Biol 40:207–215

    Google Scholar 

  • Hay ME, Kappel QE, Fenical W (1994) Synergisms in plant defenses against herbivores: interactions of chemistry, calcification, and plant quality. Ecology 75:1714–1726

    Google Scholar 

  • Heine JN, McClintock JB, Slattery M, Weston J (1991) Energetic composition, biomass, and chemical defense in the common antarctic nemertean Parborlasia corrugatus McIntosh. J Exp Mar Biol Ecol 153:15–25

    Google Scholar 

  • Hirose E (1999) Pigmentation and acid storage in the tunic: protective functions of the tunic cells in the tropical ascidian Phallusia nigra. Invertebr Biol 118:414–422

    Google Scholar 

  • Koh LL, Goh NKC, Chou LM, Tan YW (2000) Chemical and physical defenses of Singapore gorgonians (Octocorallia: Gorgonacea). J Exp Mar Biol Ecol 251:103–115

    Article  PubMed  Google Scholar 

  • Kott P (1969) Antarctic Ascidiacea. Antarct Res Ser 13:1–239

    Google Scholar 

  • Kott P (1989) Form and function in the Ascidiacea. Bull Mar Sci 45:253–276

    Google Scholar 

  • Kowalke J, Tatian M, Sahade R, Arntz W (2001) Production and respiration of Antarctic ascidians. Polar Biol 24:663–669

    Article  Google Scholar 

  • Kühne S (1997) Solitäre Ascidien in der Potter Cove (King George Island, Antarktis), ihre ökologische Bedeutung und Populationsdynamik. Rep Polar Res 252:1–153

    Google Scholar 

  • Lambert G (1979) Early post-metamorphic growth, budding and spicule formation in the compound ascidian Cystodes lobatus. Biol Bull (Woods Hole) 157:464–477

    Google Scholar 

  • Lawrence JM (1973) Level, content, and caloric equivalents of the lipid, carbohydrate and protein in the body components of Luidia clathrata (Echinodermata: Asteroidea: Platyasterida) in Tampa Bay. J Exp Mar Biol Ecol 11:263–274

    Article  CAS  Google Scholar 

  • Lindquist N, Hay ME, Fenical W (1992) Defense of ascidians and their conspicuous larvae: adult vs larval chemical defenses. Ecol Monogr 62:547–568

    Google Scholar 

  • Mahon AR, Amsler CD, McClintock JB, Amsler MO, Baker BJ (2003) Tissue-specific palatability and chemical defenses against macropredators and pathogens in the common articulate brachiopod Liothyrella uva from the Antarctic Peninsula. J Exp Mar Biol Ecol 290:197–210

    Article  CAS  Google Scholar 

  • McClintock JB (1987) Investigation of the relationship between invertebrate predation and biochemical composition, energy content, spicule armament and toxicity of benthic sponges at McMurdo Sound, Antarctica. Mar Biol 94:479–487

    CAS  Google Scholar 

  • McClintock JB (1994) The trophic biology of antarctic echinoderms. Mar Ecol Prog Ser 111:191–202

    Google Scholar 

  • McClintock JB, Baker BJ (1997a) A review of the chemical ecology of antarctic marine invertebrates. Am Zool 37:329–342

    CAS  Google Scholar 

  • McClintock JB, Baker BJ (1997b) Palatability and chemical defenses in the eggs, embryos, and larvae of shallow-water antarctic marine invertebrates. Mar Ecol Prog Ser 154:121–131

    Google Scholar 

  • McClintock JB, Baker BJ (2001) Marine chemical ecology. CRC Press, Boca Raton, Fla., USA

  • McClintock JB, Pearse JS, Bosch I (1988) Population structure and energetics of the shallow-water antarctic seastar Odontaster validus in contrasting habitats. Mar Biol 99:235–246

    Google Scholar 

  • McClintock JB, Heine J, Slattery M, Weston J (1991) Biochemical and energetic composition, population biology, and chemical defense of the antarctic ascidian Cnemidocarpa verrucosa Lesson. J Exp Mar Biol Ecol 147:163–175

    Article  CAS  Google Scholar 

  • McClintock JB, Slattery M, Thayer CW (1993) Energy content and chemical defense of the articulate brachiopod Liothyrella uva from the Antarctic Peninsula. J Exp Mar Biol Ecol 169:103–116

    CAS  Google Scholar 

  • McClintock JB, Baker BJ, Steinberg DK (2001) The chemical ecology of holoplankton and meroplankton. In: McClintock JB, Baker BJ (eds) Marine chemical ecology. CRC Press, Boca Raton, Fla., pp 195–226

  • Millar RH (1971) The biology of ascidians. Adv Mar Biol 9:1–100

    Google Scholar 

  • Moeller CB (1998) Aspects of the chemical ecology of Antarctic marine sponges. MS thesis, University of Alabama, Birmingham

  • Monteiro SM, Chapman MG, Underwood AJ (2002) Patches of the ascidian Pyura stolonifera (Heller, 1878): structure of habitat and associated intertidal assemblages. J Exp Mar Biol Ecol 270:171–189

    Article  Google Scholar 

  • Paine RT (1964) Ash and calorie determinations of sponge and opisthobranch tissue. Ecology 45:384–387

    Google Scholar 

  • Paine RT (1971) The measurement and application of the calorie to ecological problems. Annu Rev Ecol Syst 2:145–164

    Article  Google Scholar 

  • Parry DL (1984) Chemical properties of the test of ascidians in relation to predation. Mar Ecol Prog Ser 17:279–282

    CAS  Google Scholar 

  • Paul VJ (1992) Ecological role of marine natural products. Cornstock, London

  • Paul VJ, Lindquist N, Fenical W (1990) Chemical defense of the tropical ascidian Atapazoa sp. and its nudibranch predators Nembrotha spp. Mar Ecol Prog Ser 59:109–118

    CAS  Google Scholar 

  • Pawlik JR (1993) Marine invertebrate chemical defenses. Chem Rev 93:1911–1922

    CAS  Google Scholar 

  • Pawlik JR, Chanas B, Tooner RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish. I. Chemical deterrency. Mar Ecol Prog Ser 127:183–194

    CAS  Google Scholar 

  • Peterson JK, Schou O, Thor P (1995) Growth and energetics in the ascidian Ciona intestinalis. Mar Ecol Prog Ser 120:175–184

    Google Scholar 

  • Pisut DP, Pawlik JR (2002) Anti-predatory chemical defenses of ascidians: secondary metabolites or inorganic acids? J Exp Mar Biol Ecol 270:203–214

    Google Scholar 

  • Puglisi MP, Paul VJ, Biggs J, Slattery M (2002) Co-occurrence of chemical and structural defenses in the gorgonian corals of Guam. Mar Ecol Prog Ser 239:105–114

    Google Scholar 

  • Rhoades D (1979) Evolution of plant defenses against herbivores. In: Rosenthal GA, Janzen DH (eds) Herbivores. Academic, New York, pp 4–54

  • Slattery M, McClintock JB (1995) Population structure and feeding deterrence in three shallow-water Antarctic soft corals. Mar Biol 122:461–470

    Google Scholar 

  • Slattery M, McClintock JB, Heine JN (1995) Chemical defenses in antarctic soft corals: evidence for antifouling compounds. J Exp Mar Biol Ecol 190:61–77

    Google Scholar 

  • Sluiter CP (1906) Tuniciers. Expedition antarctique francaise 1903–1905, vol 6. pp 1–48

  • Smith MJ, Dehnel PA (1970) The chemical and enzymatic analyses of the tunic of the ascidian Halocynthia aurantium (Pallas). Comp Biochem Physiol 35:17–30

    Article  CAS  Google Scholar 

  • Sokal RR, Rohlf FJ (1995) Biometry. Freeman, New York

  • Stoecker D (1978) Resistance of a tunicate to fouling. Biol Bull (Woods Hole) 155:615–626

    Google Scholar 

  • Stoecker D (1980a) Chemical defenses of ascidians against predators. Ecology 61:1327–1334

    CAS  Google Scholar 

  • Stoecker D (1980b) Relationship between chemical defense and ecology in benthic ascidians. Mar Ecol Prog Ser 3:257–265

    CAS  Google Scholar 

  • Stoecker D (1980c) Distribution of acid and vanadium in Rhopalaea birkeland Tokioka. J Exp Mar Biol Ecol 48:277–281

    Article  CAS  Google Scholar 

  • Targett TE (1981) Trophic ecology and structure of coastal antarctic fish communities. Mar Ecol Prog Ser 4:243–263

    Google Scholar 

  • Tarjuelo I, Lopez-Lengentil S, Codina M, Turon X (2002) Defence mechanisms of adults and larvae of colonial ascidians: patterns of palatability and toxicity. Mar Ecol Prog Ser 235:103–115

    Google Scholar 

  • Tatian M, Sahade R, Doucet ME, Esnal GB (1998a) Some aspects of antarctic ascidians (Tunicata, Ascidiacea) of Potter Cove, King George Island. Ber Polarforsh 299:113–118

    Google Scholar 

  • Tatian M, Sahade R, Doucet ME, Esnal GB (1998b) Ascidians (Tunicata, Ascidiacea) of Potter Cove, South Shetland Islands, Antarctica. Antarct Sci 10:147–152

    Google Scholar 

  • Teo SL-M, Ryland JS (1994) Toxicity and palatability of some British ascidians. Mar Biol 120:297–303

    Google Scholar 

  • Teo SL-M, Ryland JS (1995) Potential antifouling mechanisms using toxic chemicals in some British ascidians. J Exp Mar Biol Ecol 188:49–62

    Article  CAS  Google Scholar 

  • Tugwell S, Branch GM (1989) Differential polyphenolic distribution among tissues in the kelps Eklonia maxima, Laminaria pallida and Macrocystis augustifolia in relation to plant-defense theory. J Exp Mar Biol Ecol 129:219–230

    CAS  Google Scholar 

  • van Alstyne KL, Wylie CR, Paul VJ (1994) Antipredator defenses in tropical Pacific soft corals (Coelenterata: Alcyonacea). II. The relative importance of chemical and structural defenses in three species of Sinularia. J Exp Mar Biol Ecol 178:17–34

    Article  Google Scholar 

  • Vervoort HC, Pawlik JR, Fenical W (1998) Chemical defense of the Caribbean ascidian Didemnum conchyliatum. Mar Ecol Prog Ser 164:221–228

    CAS  Google Scholar 

  • Wacasey JW, Atkinson EG (1987) Energy values of marine benthic invertebrates from the Canadian Arctic. Mar Ecol Prog Ser 39:243–250

    Google Scholar 

  • Waddell B, Pawlik JR (2000a) Defenses of Caribbean sponges against invertebrate predators. I. Assays with hermit crabs. Mar Ecol Prog Ser 195:125–132

    Google Scholar 

  • Waddell B, Pawlik JR (2000b) Defenses of Caribbean sponges against invertebrate predators. II. Assays with sea stars. Mar Ecol Prog Ser 195:133–144

    Google Scholar 

  • Young CM (1986) Defenses and refuges: alternative mechanisms of coexistence between a predatory gastropod and its ascidian prey. Mar Biol 91:513–522

    Google Scholar 

  • Young DN, Howard BM, Fenical W (1980) Subcellular localization of brominated secondary metabolites in the red alga Laurencia synderae. J Phycol 16:182–185

    CAS  Google Scholar 

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Acknowledgements

Laboratory and field assistance from K. Peters and K. Iken are gratefully acknowledged. We wish to also acknowledge and thank those individuals employed by Raytheon Polar Services Company for providing logistical support in the field. This research was facilitated by the generous support of the Office of Polar Programs of the National Science Foundation to C.D.A. and J.B.M. (OPP-9814538, OPP-0125181) and to B.J.B. (OPP-9901076, OPP-0125152). The experiments in this paper comply with the current laws of the United States.

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  1. Department of Biology, University of Alabama at Birmingham, Birmingham, AL, 35294, USA

    J. B. McClintock, M. O. Amsler, C. D. Amsler & K. J. Southworth

  2. Department of Chemistry, University of South Florida, Tampa, FL, 33620, USA

    C. Petrie & B. J. Baker

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  1. J. B. McClintock
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  2. M. O. Amsler
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  3. C. D. Amsler
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Correspondence to J. B. McClintock.

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Communicated by P.W. Sammarco, Chauvin

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McClintock, J.B., Amsler, M.O., Amsler, C.D. et al. Biochemical composition, energy content and chemical antifeedant and antifoulant defenses of the colonial Antarctic ascidian Distaplia cylindrica . Marine Biology 145, 885–894 (2004). https://doi.org/10.1007/s00227-004-1388-5

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