Fishes learn aversions to a nudibranch's chemical defense

Marine Ecology Progress Series

Volumn 307, Issue , 2006, Pages 199-208

  Long, Jeremy D ^a   Hay, Mark E ^a  

^a GEORGIA INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Chemical ecology; Fish behavior; Oyster reef; Predator prey interactions

Indexed keywords

CHEMICAL DEFENSE; CHEMICAL ECOLOGY; FISH; LEARNING; PREDATOR-PREY INTERACTION; REEF;

CALLINECTES; CALLINECTES SAPIDUS; CALLINECTES SIMILIS; CEPHALOPODA; CHASMODES BOSQUIANUS; DECAPODA (CRUSTACEA); DORIOPSILLA PHARPA; FUNDULUS HETEROCLITUS; OSTREIDAE; PANOPEUS HERBSTII; PISCES; SCOMBRIDAE GEN. SP.; SCYLLA SERRATA;

EID: 33644525352     PISSN: 01718630     EISSN: None     Source Type: Journal    
DOI: 10.3354/meps307199     Document Type: Article

References (63)

1. Avila C (1995) Natural products of opisthobranch mollusks: a biological review. Oceanogr Mar Biol Annu Rev 33:487-559
2. Avila C, Paul VJ (1997) Chemical ecology of the nudibranch Glossodoris pallida: is the location of diet-derived metabolites important for defense? Mar Ecol Prog Ser 150:171-180
3. Barnes CS, Loder JW (1962) Structure of polygodial: a new sesquiterpene dialdehyde from Polygonum hydropiper. Aust J Chem 15:322-327
4. Barry JP, Baxter CH, Sagarin RD, Gilman SE (1995) Climate-related, long-term faunal changes in a California rocky intertidal community. Science 267:672-675
5. Berenbaum MR, Miliczky E (1984) Mantids and milkweed bugs - efficacy of aposematic coloration against invertebrate predators. Am Midl Nat 111:64-68
6. Bernays EA, Chapman RF (2000) Plant secondary compounds and grasshoppers: beyond plant defenses. J Chem Ecol 26:1773-1794
7. Bernstein IL (1978) Learned taste aversions in children receiving chemotherapy. Science 200:1302-1303
8. Burghardt GM, Wilcoxon HC, Czaplick JA (1973) Conditioning in garter snakes - aversion to palatable prey induced by delayed illness. Anim Learn Behav 1:317-320
9. Cauley MJ, Schluter D (2003) Predators favor mimicry in a tropical reef fish. Proc R Soc Ser B 270:667-672
10. Cimino G, Ghiselin M (1999) Chemical defense and evolutionary trends in biosynthetic capacity among dorid nudibranchs (Mollusca: Gastropods: Opisthobranchia). Chemoecology 9:187-207
11. Cimino G, Derosa S, Destefano S, Sodano G (1982) The chemical defense of four Mediterranean nudibranchs. Comp Biochem Physiol B 73:471-474
12. Cimino G, Derosa S, Destefano S, Sodano G, Villani G (1983) Dorid nudibranch elaborates its own chemical defense. Science 219:1237-1238
13. Cronin G, Hay ME (1996) Susceptibility to herbivores depends on recent history of both the plant and animal. Ecology 77:1531-1543
14. Cronin G, Hay ME, Fenical W, Lindquist N (1995) Distribution, density, and sequestration of host chemical defenses by the specialist nudibranch Tritonia hamnerorum found at high densities on the sea fan Gorgonia ventalina. Mar Ecol Prog Ser 119:177-189
15. Crossland MR (2001) Ability of predatory native Australian fishes to learn to avoid toxic larvae of the introduced toad Bufo marinus. J Fish Biol 59:319-329
16. Dethier VG, Yost MT (1979) Oligophagy and absence of food aversion learning in tobacco hornworms, Manduca sexta. Physiol Entomol 4:125-130
17. Estes JA, Tinker MT, Williams TM, Doak DF (1998) Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282:473-476
18. Eyster LS, Stancyk SE (1981) Reproduction, growth and trophic interactions of Doriopsilla pharpa Marcus in South Carolina. Bull Mar Sci 31:72-82
19. Faulkner DJ, Ghiselin MT (1983) Chemical defense and evolutionary ecology of dorid nudibranchs and some other opisthobranch gastropods. Mar Ecol Prog Ser 13:295-301
20. Garcia J, Hankins WG, Rusiniak KW (1974) Behavioral regulation of milieu interne in man and rat. Science 185:824-831
21. Gelperin A (1975) Rapid food aversion learning by a terrestrial mollusk. Science 189:567-570
22. Gerhart DJ (1984) Prostaglandin A2 - an agent of chemical defense in the Caribbean gorgonian Plexaura homomalla. Mar Ecol Prog Ser 19:181-187
23. Gerhart DJ (1991) Emesis, learned aversion, and chemical defense in octocorals - a central role for prostaglandins. Am J Physiol 260:R839-R843
24. Gerhart DJ, Coll JC (1993) Pukalide, a widely distributed octocoral diterpenoid, induces vomiting in fish. J Chem Ecol 19:2697-2704
25. Guida VG (1976) Sponge predation in oyster reef community as demonstrated with Cliona celata Grant. J Exp Mar Biol Ecol 25:109-122
26. Hay ME (1992) The role of seaweed chemical defenses in the evolution of feeding specialization and in the mediation of complex interactions. In: Paul VJ (ed) Ecological roles for marine natural products. Comstock Publishing Associates, Ithaca, NY, p 93-118
27. Hay ME (1996) Marine chemical ecology: what's known and what's next? J Exp Mar Biol Ecol 200:103-134
28. Hay ME, Stachowicz JJ, Cruz-Rivera E, Bullard S, Deal MS, Lindquist N (1998) Bioassays with marine and freshwater macroorganisms. In: Haynes KF, Millar JG (eds) Methods in chemical ecology, VoL 2. Chapman & Hall, New York, p 39-141
29. Howard RW, Blomquist GJ (2005) Ecological, behavioral, and biochemical aspects of insect hydrocarbons. Annu Rev Entomol 50:371-393
30. Kubanek J, Graziani EI, Andersen RJ (1997) Investigations of terpenoid biosynthesis by the dorid nudibranch Cadlina luteomarginata. J Org Chem 62:7239-7246
31. Kubanek J, Jensen PR, Keifer PA, Sullards C, Collins DO, Fenical W (2003) Seaweed resistance to microbial attack: a targeted chemical defense against marine fungi. Proc Natl Acad Sci USA 100:6916-6921
32. Kubo I, Ganjian I (1981) Insect antifeedant terpenes, hot-tasting to humans. Experientia 37:1063-1064
33. Laska M, Metzker K (1998) Food avoidance learning in squirrel monkeys and common marmosets. Learn Mem 5:193-203
34. Launchbaugh KL, Provenza FD (1993) Can plants practice mimicry to avoid grazing by mammalian herbivores? Oikos 66:501-506
35. Lee JC, Bernays EA (1988) Declining acceptability of a food plant for the polyphagous grasshopper Schistocerca americana: the role of food aversion learning. Physiol Entomol 13:291-301
36. Lessios HA (1988) Mass mortality of Diadema antillarum in the Caribbean - what have we learned? Annu Rev Ecol Syst 19:371-393
37. Lindquist N, Hay ME (1995) Can small rare prey be chemically defended - the case for marine larvae. Ecology 76:1347-1358
38. Long JD (2004) Plasticity of consumer-prey interactions in the sea. PhD dissertation, Georgia Institute of Technology, Atlanta, GA
39. Miller MW, Bourque AS, Bohnsack JA (2002) An analysis of the loss of acroporid corals at Looe Key, Florida, USA: 1983-2000. Coral Reefs 21:179-182
40. Miyazawa K, Noguchi T (2001) Distribution and origin of tetrodotoxin. J Toxicol Toxin Rev 20:11-33
41. Nicolaus LK, Cassel JF, Carlson RB, Gustavson CR (1983) Taste-aversion conditioning of crows to control predation on eggs. Science 220:212-214
42. Okuda RK, Scheuer PJ, Hochlowski JE, Walker RP, Faulkner DJ (1983) Sesquiterpenoid constituents of eight porostome nudibranchs. J Org Chem 48:1866-1869
43. Parker RO Jr, Dixon RL (1998) Changes in a North Carolina reef fish community after 15 years of intense fishing - global warming implications. Trans Am Fish Soc 127:909-920
44. Paul VJ, Seo Y, Cho KW, Rho JR, Shin J, Bergquist PR (1997) Sesquiterpenoids of the drimane class from a sponge of the genus Dysidea. J Nat Prod (Lloydia) 60:1115-1120
45. Pawlik JR, Kernan MR, Molinski TF, Harper MK, Faulkner DJ (1988) Defensive chemicals of the Spanish dancer nudibranch Hexabranchus sanguineus and its egg ribbons: macrolides derived from a sponge diet. J Exp Mar Biol Ecol 119:99-109
46. Pawlik JR, Chanas B, Toonen RJ, Fenical W (1995) Defenses of Caribbean sponges against predatory reef fish. 1. Chemical deterrency. Mar Ecol Prog Ser 127:183-194
47. Penney BK (2002) Lowered nutritional quality supplements nudibranch chemical defense. Oecologia 132:411-418
48. Piel J, Hui DQ, Wen GP, Butzke D, Platzer M, Fusetani N, Matsunaga S (2004) Antitumor polyketide biosynthesis by an uncultivated bacterial symbiont of the marine sponge Theonella swinhoei. Proc Natl Acad Sci USA 101:16222-16227
49. Provenza FD (1995) Tracking variable environments - there is more than one kind of memory. J Chem Ecol 21:911-923
50. Provenza FD, Villalba JJ, Dziba LE, Atwood SB, Banner RE (2003) Linking herbivore experience, varied diets, and plant biochemical diversity. Small Ruminant Res 49:257-274
51. Ratcliffe JM, Fenton MB, Galef BG (2003) An exception to the rule: common vampire bats do not learn taste aversions. Anim Behav 65:385-389
52. Rogers CN, de Nys R, Steinberg PD (2002) Effects of algal diet on the performance and susceptibility to predation of the sea hare Aplysia parvula. Mar Ecol Prog Ser 236:241-254
53. Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annu Rev Ecol Syst 31:481-531
54. Slattery MC, Avila C, Starmer J, Paul VJ (1998) A sequestered soft coral diterpene in the aeolid nudibranch Phyllodesmium guamensis. J Exp Mar Biol Ecol 226:33-49
55. Taylor RB, Lindquist N, Kubanek J, Hay ME (2003) Intraspecific variance in palatability and defensive chemistry of brown seaweeds: effects on herbivore fitness. Oecologia 136:412-423
56. Thacker RW, Nagle DG, Paul VJ (1997) Effects of repeated exposures to marine cyanobacterial secondary metabolites on feeding by juvenile rabbitfish and parrotfish. Mar Ecol Prog Ser 147:21-29
57. Thacker RW, Becerro MA, Lumbang WA, Paul VJ (1998) Allelopathic interactions between sponges on a tropical reef. Ecology 79:1740-1750
58. Villalba JJ, Provenza FD, Han GD (2004) Experience influences diet mixing by herbivores: implications for plant biochemical diversity. Oikos 107:100-109
59. Warburton K (2003) Learning of foraging skills by fish. Fish Fish 4:203-215
60. Wilcoxon HC, Dragoin WB, Kral PA (1971) Illness induced aversions in rat and quail: relative salience of visual and gustatory cues. Science 171:826-828
61. Yoerg SI (1991) Social feeding reverses learned flavor aversions in spotted hyenas (Crocuta crocuta). J Comp Psychol 105:185-189
62. Young CM, Bingham BL (1987) Chemical defense and aposomatic coloration in larvae of the ascidian Ecteinascidia turbinata. Mar Biol 96:539-544
63. Zar JH (1999) Biostatistical analysis. 4th edn. Prentice-Hall, Upper Saddle River, NJ