Multiple components in ink of the sea hare Aplysia californica are aversive to the sea anemone Anthopleura sola

Journal of Experimental Marine Biology and Ecology

Volumn 334, Issue 2, 2006, Pages 256-268

  Kicklighter, Cynthia E ^a   Derby, Charles D ^a  

^a Georgia State University   (United States)

Author keywords

Chemical defense; Opaline; Predator prey

Indexed keywords

BEHAVIORAL RESPONSE; CHEMICAL DEFENSE; FEEDING BEHAVIOR; MOLLUSC CULTURE; PREDATION RISK; PROTECTIONISM; PROTEIN;

ACTINIARIA; ALGAE; ANASPIDEA; ANEMONE; ANTHOPLEURA; ANTHOPLEURA SOLA; APLYSIA; APLYSIA CALIFORNICA; GRACILARIA; GRACILARIA FEROX;

EID: 33646926756     PISSN: 00220981     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jembe.2006.02.002     Document Type: Article

References (52)

1. Ambrose H.W., and Givens R.P. Distastefulness as a defense mechanism in Aplysia brasiliana (Mollusca: Gastropoda). Mar. Behav. Physiol. 6 (1979) 57-64
2. Appleton D.R., Babcock R.C., and Copp B.R. Novel tryptophan-derived dipeptides and bioactive metabolites from the sea hare Aplysia dactylomela. Tetrahedron 57 (2001) 10181-10189
3. Butzke D., Hurwitz R., Thiede B., Goedert S., and Rudel T. Cloning and biochemical characterization of APIT, a new l-amino acid oxidase from Aplysia punctata. Toxicon 46 (2005) 479-489
4. Carefoot T.H. Aplysia: its biology and ecology. J. Exp. Biol. 24 (1987) 167-284
5. Carefoot T.H., Pennings S.C., and Danko J.P. A test of novel function(s) for the ink of sea hares. J. Exp. Mar. Biol. Ecol. 234 (1999) 185-197
6. Christomanos A. Nature of the pigment of A. depilans. Nature 175 (1955) 310
7. Deal M.S., Hay M.E., Wilson D., and Fenical W. Glactolipids rather than phlorotannins as herbivore deterrents in the brown seaweed Fucus vesiculosis. Oecologia 136 (2003) 107-114
8. DiMatteo T. The inking behavior of Aplysia dactylomela (Gastropoda: Opisthobranchia): evidence for distastefulness. Mar. Behav. Physiol. 7 (1981) 285-290
9. DiMatteo T. The ink of Aplysia dactylomela (Rang, 1828) (Gastropoda: Opisthobranchia) and its role as a defensive mechanism. J. Exp. Mar. Biol. Ecol. 57 (1982) 169-180
10. Faulkner D.J. Chemical defenses of marine molluscs. In: Paul V.J. (Ed). Ecological Roles of Marine Natural Products (1992), Comstock Publishing Associates, Ithaca 119-163
11. Ginsburg D.W., and Paul V.J. Chemical defenses in the sea hare Aplysia parvula: importance of diet and sequestration of algal secondary metabolites. Mar. Ecol. Prog. Ser. 215 (2001) 261-274
12. Hay M.E. Predictable spatial escapes from herbivory: how do these affect the evolution of herbivore resistance in tropical marine communities?. Oecologia 64 (1984) 396-407
13. Hay M.E., Duffy J.E., Pfister C.A., and Fenical W. Chemical defense against different marine herbivores: are amphipods insect equivalents?. Ecology 68 (1987) 1567-1580
14. Johnson, P.M., 2002. Multi-component chemical defense in sea hares (Gastropoda: Opisthobranchia): antipredator compounds act as both honest and deceptive signals to multiple predator species. Ph.D. Dissertation, University of Washington.
15. Johnson P.M., and Willows A.O.D. Defense in sea hares (Gastropoda, Opisthobranchia, Anaspidea): multiple layers of protection from egg to adult. Mar. Freshw. Behav. Physiol. 32 (1999) 147-180
16. Johnson P.M., Kicklighter C.E., Schmidt M., Kamio M., Yang H., Elkin D., Michel W.C., Tai P.C., and Derby C.D. Packaging of chemicals in the defensive secretory glands of the sea hare Aplysia californica. J. Exp. Biol. 209 (2006) 78-88
17. Kicklighter, C.E., Hay, M.E., (submitted for publication). Avoiding versus deterring consumers: interactions among defensive and escape strategies in sabellid worms. Oecologia.
18. Kicklighter C.E., Kubanek J., Barsby T., and Hay M.E. Palatability and defense of some tropical infaunal worms: alkylpyrrole sulfamates as deterrents to fish feeding. Mar. Ecol. Prog. Ser. 263 (2003) 299-306
19. Kicklighter C.E., Shabani S., Johnson P.M., and Derby C.D. Sea hares use novel antipredatory chemical defenses. Curr. Biol. 15 (2005) 549-554
20. Kinnel R.B., Dieter R.K., Meinwald J., Van Engen D., Clardy J., Eisner T., Stallard M.O., and Fenical W. Brasilenyne and cis-dihydrorhodophytin: antifeedant medium-ring haloether from a sea hare (Aplysia brasiliana). Proc. Natl. Acad. Sci. U.S.A. 76 (1979) 3576-3579
21. Kupchan S.M., Britton R.W., Lacadie J.A., Ziegler M.F., and Sigel C.W. The isolation and structural elucidation of bruceantin and bruceantinol. J. Org. Chem. 40 (1975) 648-654
22. Lindstedt K.J. Biphasic feeding response in a sea anemone: control by asparagine and glutathione. Science 173 (1971) 333-334
23. Lubchenco J., and Gaines S.D. A unified approach to marine plant-herbivore interactions: I. Populations and communities. Annu. Rev. Ecolog. Syst. 12 (1981) 405-437
24. Lucero M.T., Farrington H., and Gilly W.F. Quantification of l-dopa and dopamine in squid ink-implications for chemoreception. Biol. Bull. 187 (1994) 55-63
25. Lukasheva E.V., and Berezov T.T. l-Lysine α-oxidase: physicochemical and biological properties. Biochemistry (Mosc.) 67 (2002) 1152-1158
26. MacColl R., Galivan J., Berns D.S., Nimec Z., Guard-Friar D., and Wagoner D. The chromophore and polypeptide composition of Aplysia ink. Biol. Bull. 179 (1990) 326-331
27. Nishibori K. Studies on the pigments of marine animals: IX. Pigments of the sea-slug Aplysia kurodai. Publ. Seto Mar. Biol. Lab. 8 (1960) 327-335
28. Nolen T.G., Johnson P.M., Kicklighter C.E., and Capo T. Ink secretion by the marine snail Aplysia californica enhances its ability to escape from a natural predator. J. Comp. Physiol., A Sens. Neural Behav. Physiol. 176 (1995) 239-254
29. Paul V.J., and Pennings S.C. Diet-derived chemical defenses in the sea hare Stylocheilus longicauda (Quoy et Gaimard 1824). J. Exp. Mar. Biol. Ecol. 151 (1991) 227-243
30. Paul V.J., and Van Alstyne K.L. Use of ingested algal diterpenoids by Elysia halimedae Macnae (Opisthobranchia: Ascoglossa) as anti-predator defenses. J. Exp. Mar. Biol. Ecol. 119 (1988) 15-29
31. Pawlik J.R., and Fenical W. A re-evaluation of the ichthyodeterrent role of prostaglandins in the Caribbean gorgonian coral Plexaura homomalla. Mar. Ecol. Prog. Ser. 52 (1989) 95-98
32. Pearse V., and Francis L. Anthopleura sola, a new species, solitary sibling species to the aggregating sea anemone, A. elegantissima (Cnidaria: Anthozoa: Actiniaria: Actiniidae). Proc. Biol. Soc. Wash. 113 (2000) 596-608
33. Pennings S.C. Interspecific variation in chemical defense in the sea hare (Opisthobranchia: Anaspidea). J. Exp. Mar. Biol. Ecol. 180 (1994) 203-219
34. Pennings S.C., and Paul V.J. Sequestration of dietary secondary metabolites by three species of sea hares: location, specificity and dynamics. Mar. Biol. 117 (1993) 535-546
35. Pennings S.C., Paul V.J., Dunbar D.C., Hamann M.T., Lumbang W.A., Novack B., and Jacobs R.S. Unpalatable compounds in the amrine gastropod Dolabella auricularia: distribution and effect of diet. J. Chem. Ecol. 25 (1999) 735-755
36. Prince J., Nolen T.G., and Coelho L. Defensive ink pigment processing and secretion in Aplysia californica: concentration and storage of phycoerythrobilin in the ink gland. J. Exp. Biol. 201 (1998) 1595-1613
37. Rogers C.N., De Nys R., Charlton T.S., and Steinberg P.D. Dynamics of algal secondary metabolites in two species of sea hare. J. Chem. Ecol. 26 (2000) 721-743
38. Setchell W.A., and Gardner N.L. The Marine Algae of the Pacific Coast of North America (1967), Wheldon and Wesley, Ltd., New York 898 pp.
39. Smith G.M. Marine Algae of the Monterey Peninsula California. 2nd ed. (1969), Stanford University Press, Stanford, CA 752 pp.
40. Stallard M.O., and Faulkner D.J. Chemical constituents of the digestive gland of the sea hare Aplysia californica: I. Importance of diet. Comp. Biochem. Physiol. 49B (1974) 25-35
41. Stallard M.O., and Faulkner D.J. Chemical constituents of the digestive gland of the sea hare Aplysia californica: II. Chemical transformations. Comp. Biochem. Physiol. 49B (1974) 37-41
42. Takamatsu S., Hodges T.W., Rajbhandari I., Gerwick W.H., Hamann M.T., and Nagle D.G. Marine natural products as novel antioxidant prototypes. J. Nat. Prod. 66 (2003) 605-608
43. Thompson T.E. Defensive adaptations in opisthobranchs. J. Mar. Biol. Assoc. U.K. 39 (1960) 123-134
44. Tritt S.H., and Byrne J.H. Motor controls of opaline secretion in Aplysia californica. J. Neurophysiol. 43 (1980) 581-594
45. Troxler R.R., Offner G.D., and Capo T.R. Structural studies on aplysioviolin. Biol. Bull. 161 (1981) 339
46. Walters E.T., and Erickson M.T. Directional control and the functional organization of defensive responses in Aplysia. J. Comp. Physiol., A Sens. Neural Behav. Physiol. 159 (1986) 339-351
47. Walters E.T., Illich P.A., and Hickie C. Inking and siphon response plasticity in Aplysia. Anti-predator and alarm signal functions. Soc. Neurosci. Abstr. 9 (1993) 578
48. Wellner D., and Meister A. Studies on the mechanism of action of l-amino acid oxidase. J. Biol. Chem. 236 (1961) 2357-2364
49. Winkler L.R. Distribution of organic bromine compounds in Aplysia californica Cooper, 1863. Veliger 2 (1969) 268-271
50. Winkler L.R., and Tilton B.E. 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. Pac. Sci. 16 (1962) 286-290
51. Yamada K., and Kigoshi H. Bioactive compounds from the sea hares of two genera: Aplysia and Dolabella. Chem. Soc. Jpn. 70 (1997) 1479-1489
52. Yang H., Johnson P.M., Ko K.C., Kamio M., Germann M.W., Derby C.D., and Tai P.C. Cloning, characterization and expression of escapin, a broadly antimicrobial FAD-containing l-amino acid oxidase from ink of the sea hare Aplysia californica. J. Exp. Biol. 208 (2005) 3609-3622