Abstract
-
1.
Aplysia californica incorporates toxins and pigments from its red seaweed diet into its body and ink, purportedly as a defense against predation. We tested ink's potential defensive function by assessing the survival of green seaweed-fed (red algal toxin deprived) snails in encounters with a natural predator, the sea anemone Anthopleura xanthogrammica.
-
2.
Red seaweed-fed Aplysia secreted copious amounts of ink when ensnared in anemone tentacles. A similar amount of ink applied to “inkless” (green-fed) snails as they were engulfed by an anemone enhanced their survival [71% survived (ink) vs 7% (seawater control)]. Ink caused anemones to reject whitefish (a familiar food) [50% rejected (ink) vs 10% (seawater control)], triggering gastrovascular eversions, which ejected ink as well as prey from their digestive cavities. Snails with only a passive chemical defense (algal toxins, no ink) escaped less often than snails with only an active chemical defense (ink, no red algal toxins) (20% survived vs 71%) and about as often as “red algal toxin deprived” snails (20% vs 12%). Snails avoided ink by chemical orientation, thus avoiding potential sites of ongoing predation.
-
3.
The survival value of ink and the snail's aversion to it supports ink's proposed anti-predator function.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
References
Alcock J (1993) Animal behavior: An evolutionary approach. 5th Edition. Sinauer Press, Sunderland MA
Ambrose HW, Givens RP, Chen R, Ambrose KP (1979) Distastefulness as a defense mechanism in Aplysia brasiliana (Mollusca: Gastropoda). Mar Behav Physiol 6: 57–64
Bebbington A (1977) Aplysiid species from eastern Australia with a note on the Pacific ocean Aplysiomorpha (Gastropoda, Opisthobranchia). Trans Zool Soc Lond 34: 87–147
Blankenship JE, Langlais PJ, Kittredge JS (1975) Identification of a cholinomimetic compound in the digestive gland of Aplysia californica. Comp Biochem Physiol 51(C): 129–137
Brown JL (1987) Helping and communal breeding in birds: ecology and evolution. Princeton Univ Press, Princeton NJ
Burian RM (1992) Adaptation: Historical perspectives. In: Keller EF, Lloyd EA (eds) Keywords in evolutionary biology. Harvard Univ Press, Cambridge, pp 7–12
Byrne JH (1980a) Analysis of ionic conductance mechanisms in motor cells mediating inking behavior in Aplysia californica. J Neurophysiol 43: 630–650
Byrne JH (1980b) Neural circuit for inking behavior in Aplysia californica. J Neurophysiol 43: 896–911
Byrne JH (1980c) Quantitative aspects of the contribution of ionic conductance mechanisms contributing to firing patterns of motor cells mediating inking behavior in Aplysia californica. J Neurophysiol 43: 651–668
Byrne JH (1987) Cellular analysis of associative learning. Physiol Rev 67(2): 329–439
Byrne JH, Shapiro E, Dieringer N, Koester J (1979) Biophysical mechanisms contributing to inking behavior in Aptysia. J Neurophysiol 42: 1233–1250
Carefoot T (1987) Aplysia: Its biology and ecology. Oceanogr Mar Biol Annu Rev 25: 167–284
Carew TJ, Kandel E (1977a) Inking in Aplysia californica I. Neural circuit of an all-or-none behavioral response. J Neurophysiol 40(3): 692–707
Carew TJ, Kandel ER (1977b) Inking in Aplysia californica II. Central program for inking. J Neurophysiol 40: 708–720
Carew TJ, Kandel ER (1977c) Inking in Aplysia californica III. Two different sympatric conductance mechanisms of triggering central program for inking. J Neurophysiol 40: 721–734
Carew TJ, Sahley CL (1986) Invertebrate learning and memory. From behavior to molecules. Annu Rev Neurosci 9: 435–487
Carew TJ, Hawkins RD, Kandel ER (1983) Differential classical conditioning of a defensive withdrawal reflex in Aplysia californica. Science 219: 397–400
Carew TJ, Hawkins RD, Abrams TW, Kandel ER (1984) A test of Hebb's postulate at identified synapses which mediate classical conditioning in Aplysia. J Neurosci 4(5): 1217–1224
Carew TJ, Marcus EA, Nolen TG, Rankin CH, Stopfer M (1990) The development of learning and memory in Aplysia. In: McGaugh JL, Weinberger NM, Lynch G (eds) Brain organization and memory. Cells, systems and circuits. Oxford University Press, New York NY, pp 27–51
Chapman D, Fox D (1969) Bile pigment metabolism in the sea-hare Aplysia. J Exp Mar Biol Ecol 4: 71–78
Christomanos A (1955) Nature of the pigment of Aplysia depilans. Nature 175: 310
Cohen-Bazire G, Bryant DA (1982) Phycobilisomes: Composition and structure. In: Carr NG, Whitton BA (eds) The Biology of cyanobacteria. University of California Press, Berkeley, pp 143–189
Danse B, Minale R, Riccio R, Amico V, Oriente G, Piatelli M, Trangali C, Fattorusso E, Magno S, Mayol L (1977) Further perhydroazulene diterpenes from marine organisms. Experientia 15: 412–415
Darling S, Cosgrove RE (1966) Marine natural products. I. The search for Aplysia terpenoids in red algae. The Veliger 8(3): 178–179
Dawkins M (1986) Unravelling animal behaviour. The Longman Group Limited, Essex, England
DiMatteo T (1981) The inking behavior of Aplysia dactylomela (Gastropoda: Opisthobranchia): Evidence for distastefulness. Mar Behav Physiol 7: 285–290
DiMatteo T (1982a) The ink of Aplysia dactylomela (Rang 1828) (Gastropoda: Opisthobranchia) and its role as a defensive mechanism. J Exp Mar Biol Ecol 57: 169–180
DiMatteo T (1982b) Investigation into interspecific encounters of the sea hare Aplysia dactylomela Rang 1828. The Veliger 24(1): 72–75
Eales NB (1960) Revision of the world species of Aplysia (Gastropoda, Opisthobranchia). Zoology 5(10): 267–404
Fenical W (1975) Halogenation in the Rhodophyta: A review. J Phycol 11: 245–259
Finer J, Clardy J, Fenical W, Minale L, Riccio R, Battaile J, Kirkup M, Moore RE (1979) Structures of dicyodial and dictyolactone, unusual marine diterpenoids. J Org Chem 44: 2044–2047
Fiorito G, Gherardi F (1990) Behavioural changes induced by ink in Aplysia fasciata (Mollusca, Gastropoda): Evidence for a social signal role of inking. Mar Behav Physiol 17: 129–135
Gantt E, Lipschultz CA, Grabowski J, Zimmerman PB (1979) Phycobilisomes from blue-green and red algae. Isolation criteria and dissociation characteristics. Plant Physiology 63: 615–620
Grier JW, Burk T (1992) Biology of animal behavior. 2nd Ed. Mosby-Year Book, St Louis
Hamilton WD (1964) The evolution of social behavior. J Theor Biol 7: 1–52
Hawkins RD, Abrams TW, Carew TJ, Kandel ER (1983) Differential classical conditioning of a defensive withdrawal reflex in Aplysia californica. Science 219: 397–405
Huxley J (1942) Evolution, the modern synthesis. Harpers, New York
Hyman LH (1940) The invertebrates Vol I.: Protozoa through Ctenphora. McGraw-Hill Book Co, New York
Illich PA, Hickie C, Joynes RL, Walters ET (1993) Inhibition and facilitation of competing siphon responses in Aplysia following noxious stimulation. Soc Neurosci Abstr 19: 578
Illich PA, Joynes RL, Walters ET (1994) Response-specific inhibition during general facilitation of defensive responses in Aplysia. Behav Neurosci 108: 614–623
Irie T, Suzuki M, Hayakawa Y (1969) Isolation of aplysin, debromoaplysin and aplysinol from Laurencia okamurai. Yamada Bull Chem Soc Japan 42: 843–844
Johnson PM (1994) Chemical defense in the gastropod mollusc Aplysia. Honors Senior Thesis, Department of Biology, University of Miami
Johnson PM, Nolen TG (1991) Conspecific ink is aversive to juvenile Aplysia californica. Am Zool 1(5): 112A
Johnson PM, Evoy WH, Nolen TG (1993) Distributed, mechanical stimulation of the skin triggers ink release in Aplysia. Soc Neurosci Abstr 19: 167
Kandel ER (1979) Behavioral biology of Aplysia. Freeman and Co, San Francisco CA
Kempf SC (1981) Long-lived larvae of the gastropod Aplysia juliana: Do they disperse and metamorphose or just slowly fade away? Mar Ecol Prog Ser 6: 61–65
Kicklighter CE, Johnson PM, Nolen TG (1992) Chemically mediated defensive inking in Aplysia californica. Soc Neurosci Abstr 18: 346
Kicklighter CE, Johnson PM, Robinson S, Agustines M, Nolen TG (1993) Ink release by Aplysia enhances its ability to escape from a natural predator. Soc Neurosci Abstr 19: 167
Kinnel RB, Dieter RK, Meinwald J, Van Engen D, Clardy J, Eisner T, Stallard MO, Fenical W (1979) Brasilenyne and cis-dihydro-rhodophytin: Antifeedant medium-ring haloethers from a sea hare (Aplysia brasiliana). Proc Natl Acad Sci USA 76(8): 3576–3579
Klein M, Kandel ER (1980) Mechanism of calcium current modulation underlying presynaptic facilitation and behavioral sensitization in Aplysia. Proc Natl Acad Sci USA 77(11): 6912–6916
Krauth J (1988) Distribution-free statistics: An application-oriented approach. Elsevier, New York
Kriegstein AR (1977) Stages in the post-hatching development of Aplysia californica. J Exp Zool 199(2): 275–288
Kupfermann I, Carew TJ (1974) Behavior patterns of Aplysia californica in its natural environment. Behav Biol 12: 317–337
Leonard J, Lukowiak K (1986) The behavior of Aplysia californica Cooper: I. Ethogram. Behaviour 98: 320–360
MacColl R, Galivan J, Berns DS, Nimec Z, Guard-Friar D, Wagoner D (1990) The chromophore and polypeptide composition of Aplysia ink. Biol Bul 179(3): 326–331
MacGinitie GE, MacGinitie N (1968) Natural history of marine animals. McGraw-Hill Book Company, New York
Marcus EA, Nolen TG, Rankin CH, Carew TJ (1988) Behavioral dissociation of dishabituation, sensitization and inhibition in the siphon withdrawal reflex of adult Aplysia. Science 241: 210–213
Mianmanus R (1988) Induction of settlement and metamorphosis in larvae of Aplysia brasiliana and Strombus gigas (Mollusca: Gastropoda). PhD thesis, Rosenstiel School of Marine and Atmospheric Science, University of Miami
Minale L, Raffaele R (1976) Constituents of the digestive gland of the molluscs of the genus Aplysia. I. Novel diterpenes for Aplysia depilans. Tet Lett 31: 2711–2714
Nolen TG, Carew TJ (1988) The cellular analog of sensitization in Aplysia emerges at the same time in development as behavioral sensitization. J Neurosci 8: 212–222
Paine RT (1963) Food recognition and predation on opisthobranchs by Navanax inermis (Gastropoda: Opisthobranchia). Veliger 6: 1–9
Pennings SC (1990a) Multiple factors promoting narrow host rage in the sea hare, Aplysia californica. Oecologia 82: 192–200
Pennings SC (1990b) Predator-prey interactions in opisthobranch gastropods: effects of prey body size and habitat complexity. Mar Ecol Prog Ser 62: 95–101
Rankin CH, Carew TJ (1988) Dishabituation and sensitization emerge as separate processes during development in Aplysia. J Neurosci 8(1): 197–211
Roeder K (1967) Nerve cells and insect behavior. Harvard Univ Press, Cambridge
Sargent TD (1976) Legion of night: The underwing moths. Univ Massachusetts Press, Amherst MA
Shapiro E, Koester J, Byrne JH (1979) Aplysia ink release: central locus for selective sensitivity to long duration stimuli. J Neurophysiol 42: 1223–1232
Sherman P (1985) Alarm calls of Belding's ground squirrel to aerial predators: nepotism or self-preservation? Behav Ecol Sociobiol 17: 313–323
Sokal RR, Rohlf FJ (1981) Biometry. W.H. Freeman, San Francisco CA
Stallard MO, Faulkner DJ (1974a) Chemical constituents of the digestive gland of the sea hare Aplysia californica. I. Importance of the diet. Comp Biochem Physiol B 49: 25–35
Stallard MO, Faulkner DK (1974b) Chemical constituents of the digestive gland of the sea hare Aplysia californica. II. Chemical transformations. Comp Biochem Physiol B 49: 37–41
Stopfer M, Chen X, Carew TJ (1993) Evoked ink release in Aplysia produces inhibition of the siphon withdrawal reflex in neighboring conspecifics. Behav Neural Biol 60: 196–202
Strenth NE, Blankenship JE (1978) Laboratory culture, metamorphosis and development of Aplysia brasiliana Rang, 1928 (Gastropoda: Opisthobranchia). The Veliger 21: 99–103
Switzer-Dunlap M (1978) Larval biology and metamorphosis of aplysiid gastropods. In: Chia FS, Rice ME (eds) Settlement and metamorphosis of marine invertebrate larvae. Elsevier, New York, pp 197–206
Tinbergen N (1967) Adaptive features of the black-headed gull Larus ridibundus. Proc 14th International Ornithological Congress, pp 43–59
Tobach E, Gold P, Ziegler A (1965) Preliminary observations of the inking behavior of Aplysia (Varria). The Veliger 8: 16–18
Tobach E, Zaferes A, Migenis-Lopez L (1989) Aplysia ink and opaline: exploration of their relation to predation. Bull Mar Sci 45(3): 664–670
Walters ET, Erickson MT (1986) Directional control and the functional organization of defensive responses in Aplysia. J Comp Physiol A 159: 339–351
Walters ET, Carew TJ, Kander ER (1981) Associative learning in Aplysia: Cellular correlates supporting a conditioned fear hypothesis. Science 211: 501–506
Walters ET, Illich PA, Hickie C (1993) Inking and siphon response plasticity in Aplysia: anti-predator and alarm signal functions. Soc Neurosci Abstr 19: 578
Watson M (1973) Midgut gland toxins of Hawaiian sea hares I. Isolation and preliminary toxicological observations. Toxicon 11: 259–267
Watson M, Rayner MD (1973) Midgut gland toxins of Hawaiian sea hares. II. A preliminary pharmacological study. Toxicon 11: 269–276
West-Eberhard MJ (1992) Adaptation: current uses. In: Keller EF, Lloyd EA (eds) Keywords in evolutionary biology. Harvard Univ Press, Cambridge, pp 13–18
Winkler LR (1961) Preliminary tests of the toxin extracted from California sea hares of the genus Aplysia. Pacific Science 15: 211–214
Winkler LR (1969) Distribution of organic bromine compounds in Aplysia californica Cooper 1863. The Veliger 11(3): 268–271
Winkler LR, Tilton BE (1962) Predation on the California sea hare, Aplysia californica Cooper, by the solitary great green sea anemone, Anthopleura xanthogrammica (Brandt), and the effect of sea hare toxin and acetylcholine on anemone muscle. Pacific Science 16: 286–290
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Nolen, T.G., Johnson, P.M., Kicklighter, C.E. et al. Ink secretion by the marine snail Aplysia californica enhances its ability to escape from a natural predator. J Comp Physiol A 176, 239–254 (1995). https://doi.org/10.1007/BF00239926
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00239926