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Neural Processing, Perception, and Behavioral Responses to Natural Chemical Stimuli by Fish and Crustaceans

Journal of Chemical Ecology volume 34, pages 898–914 (2008)Cite this article

Abstract

This manuscript reviews the chemical ecology of two of the major aquatic animal models, fish and crustaceans, in the study of chemoreception. By necessity, it is restricted in scope, with most emphasis placed on teleost fish and decapod crustaceans. First, we describe the nature of the chemical world perceived by fish and crustaceans, giving examples of the abilities of these animals to analyze complex natural odors. Fish and crustaceans share the same environments and have evolved some similar chemosensory features: the ability to detect and discern mixtures of small metabolites in highly variable backgrounds and to use this information to identify food, mates, predators, and habitat. Next, we give examples of the molecular nature of some of these natural products, including a description of methodologies used to identify them. Both fish and crustaceans use their olfactory and gustatory systems to detect amino acids, amines, and nucleotides, among many other compounds, while fish olfactory systems also detect mixtures of sex steroids and prostaglandins with high specificity and sensitivity. Third, we discuss the importance of plasticity in chemical sensing by fish and crustaceans. Finally, we conclude with a description of how natural chemical stimuli are processed by chemosensory systems. In both fishes and crustaceans, the olfactory system is especially adept at mixture discrimination, while gustation is well suited to facilitate precise localization and ingestion of food. The behaviors of both fish and crustaceans can be defined by the chemical worlds in which they live and the abilities of their nervous systems to detect and identify specific features in their domains. An understanding of these worlds and the sensory systems that provide the animals with information about them provides insight into the chemical ecology of these species.

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References

  • Abramson, C. I., and Feinman, R. D. 1988. Classical conditioning of the eye withdrawal reflex in the green crab. J. Neurosci 8:2907–2912.

    PubMed  CAS  Google Scholar 

  • Ache, B. W., and Young, J. M. 2005. Olfaction: diverse species, conserved principles. Neuron 48:417–430.

    PubMed  CAS  Google Scholar 

  • Appelt, C. A., and Sorensen, P. W. 2007. Female goldfish signal spawning readiness by altering when and where they release a urinary pheromone. Anim. Behav 74:1329–1338.

    Google Scholar 

  • Archdale, M. V., and Anraku, K. 2005. Feeding behavior in Scyphozoa, Crustacea and Cephalopoda. Chem. Senses 30:i303–i304.

    PubMed  Google Scholar 

  • Arnesen, A. M., and Stabell, O. B. 1992. Behaviour of stream-dwelling brown trout towards odours present in home stream water. Chemoecology 3:94–100.

    Google Scholar 

  • Asai, N., Fusetani, N., Matsunaga, S., and Sasaki, J. 2000. Sex pheromones of the hair crab Erimacrus isenbeckii. Part 1: Isolation and structures of novel ceramides. Tetrahedron 56:9895–9899.

    CAS  Google Scholar 

  • Atema, J. 1977. Functional separation of smell and taste in fish and Crustacea, pp. 165–174, in J. Le Magnen, and P. Mac Leod (eds.). Olfaction and Taste VI. Information Retrieval, Paris.

    Google Scholar 

  • Atema, J. 1988. Distribution of chemical stimuli, pp. 29–56, in J. Atema, R. R. Fay, A. N. Popper, and W. N. Tavolga (eds.). Sensory Biology of Aquatic Animals. Springer, New York.

    Google Scholar 

  • Atema, J. 1996. Eddy chemotaxis and odor landscapes: exploration of nature with animal sensors. Biol. Bull 191:129–138.

    Google Scholar 

  • Atema, J., and Steinbach, M. A. 2007. Chemical communication in the social behavior of the lobster, Homarus americanus, and other decapod Crustacea, pp. 115–144, in E. Duffy, and M. Thiel (eds.). Ecology and Evolution of Social Behavior: Crustaceans as Model Systems. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Atema, J., Holland, K., and Ikehara, W. 1980. Olfactory responses of yellowfin tuna (Thunnus albacares) are prey odors: chemical search image. J. Chem. Ecol 6:457–465.

    Google Scholar 

  • Bardach, J. E., Todd, J. H., and Crickmer, R. 1967. Orientation by taste in fish of the genus Ictalurus. Science 155:1276–1278.

    PubMed  CAS  Google Scholar 

  • Behringer, D. C., Butler, M. J., and Shields, J. D. 2006. Avoidance of disease by social lobsters. Nature 441:421.

    PubMed  CAS  Google Scholar 

  • Belanger, R. M., and Moore, P. A. 2006. The use of the major chelae by reproductive male crayfish (Orconectes rusticus) for discrimination of female odours. Behaviour 143:713–731.

    Google Scholar 

  • Berger, D. K., and Butler, M. J. 2001. Octopuses influence den selection by juvenile Caribbean spiny lobster. Mar. Freshw. Res 52:1049–1053.

    Google Scholar 

  • Bitterman, M. E. 1982. Migration and learning in fishes, pp. 397–420, in J. D. McCleave, G. P. Arnold, J. J. Dodson, and W. Neill (eds.). Mechanisms of Migration in Fishes. Plenum, New York.

    Google Scholar 

  • Bouwma, P. 2007. Should I stay or should I go? The ontogeny of spiny lobster responses to alarm odor cues. Abstract at the 2007 Benthic Ecology meeting.

  • Bouwma, P., and Hazlett, B. A. 2001. Integration of multiple predator cues by the crayfish Orconectes propinquus. Anim. Behav 61:771–776.

    Google Scholar 

  • Breithaupt, T. 2001. The fan organs of crayfish enhance chemical information flow. Biol. Bull 200:150–154.

    PubMed  CAS  Google Scholar 

  • Breithaupt, T., and Atema, J. 2000. The timing of chemical signaling with urine in dominance fights of male lobsters (Homarus americanus). Behav. Ecol. Sociobiol 49:67–78.

    Google Scholar 

  • Breithaupt, T., and Eger, P. 2002. Urine makes the difference: chemical communication in fighting crayfish made visible. J. Exp. Biol 205:1221–1231.

    PubMed  Google Scholar 

  • Briones-fourzán, P., and Lozano-álvarez, E. 2005. Seasonal variations in chemical response to conspecific scents in the spotted spiny lobster, Panulirus guttatus. N. Z. J. Mar. Freshw. Res 39:383–390.

    Google Scholar 

  • Brown, G. E., Chivers, D. P., and Smith, R. J. F. 1993. Localized defecation by pike: a response to labeling by cyprinid alarm pheromone? Behav. Ecol. Sociobiol 36:105–110.

    Google Scholar 

  • Brown, G. E., Adrian, J. C., Smyth, E., Leet, H., and Brennan, S. 2000. Ostariophysan alarm pheromones: laboratory and field tests of the functional significance of nitrogen oxides. J. Chem. Ecol 26:139–154.

    CAS  Google Scholar 

  • Brown, G. E., Adrian, J. C., Naderi, N. T., Harvey, M. C., and Kelly, J. M. 2003. Nitrogen oxides elicit antipredator responses in juvenile catfish but not convict cichlids or rainbow trout: conservation of the ostariophysan alarm pheromone. J. Chem. Ecol 29:1781–1796.

    PubMed  CAS  Google Scholar 

  • Caldwell, R., and Dingle, J. 1985. A test of individual recognition in the stomatopod Gonodactylus festae. Anim. Behav 33:101–106.

    Google Scholar 

  • Caprio, J., and Derby, C. D. 2007. Aquatic animal models in the study of chemoreception, in A. Basbaum, M. Bushnell, D. Smith, G. Beauchamp, S. Firestein, P. Dallos, D. Oertel, R. Masland, T. Albright, J. Kaas, and E. Gardner (eds.). The Senses: A Comprehensive Reference, Six-Volume Set. Elsevier, New York.

    Google Scholar 

  • Caprio, J. C., Brand, J. B., Teeter, J. H., Valentinčič, T., Kalinoski, D. L., Kohbara, J., Kamazawa, T., and Wegert, S. 1993. The taste system of the channel catfish: from biophysics to behavior. Trends Neurosci 16:192–197.

    PubMed  CAS  Google Scholar 

  • Carr, W. E. S. 1982. Chemical stimulation of feeding behavior, pp. 259–274, in T. J. Hara (ed.). Chemoreception in Fishes. Elsevier, New York.

    Google Scholar 

  • Carr, W. E. S. 1988. The molecular nature of chemical stimuli in the aquatic environment, pp. 3–27, in J. Atema, R. R. Fay, A. N. Popper, and W. N. Tavolga (eds.). Sensory Biology of Aquatic Animals. Springer, New York.

    Google Scholar 

  • Carr, W. E. S., Netherton, J. C. III, Gleeson, R. A., and Derby, C. D. 1996. Stimulants of feeding behavior in fish: analyses of tissues of diverse marine organisms. Biol. Bull 190:149–160.

    CAS  Google Scholar 

  • Caskey, J. L., and Bauer, R. T. 2005. Behavioral tests for a possible contact pheromone in the caridean shrimp Palaemonetes pugio. J. Crustac. Biol 25:571–576.

    Google Scholar 

  • Cohen, S. A. P., Hatt, H., Kubanek, J., and Mccarty, N. A. 2008. Reconstitution of a chemical defense signaling pathway in a heterologous system. J. Exp. Biol 211:599–605.

    PubMed  CAS  Google Scholar 

  • Colbourne, J. K., Singan, V. R., and Gilbert, D. G. 2005. wFleaBase: the Daphnia genome database. BMC Bioinformatics 6:45.

    PubMed  Google Scholar 

  • Corotto, F. S., Mckelvey, M. J., Parvin, E. A., Rogers, J. L., and Williams, J. M. 2007. Behavioral responses of the crayfish Procambarus clarkii to single chemosensory stimuli. J. Crustac. Biol 27:24–29.

    Google Scholar 

  • Cromarty, S. I., and Derby, C. D. 1997. Multiple receptor types on individual excitatory olfactory neurons: implications for coding of mixtures in the spiny lobster. J. Comp. Physiol. A 180:481–492.

    PubMed  CAS  Google Scholar 

  • Daniel, P. C., and Derby, C. D. 1988. Behavioral olfactory discrimination of mixtures in the spiny lobster (Panulirus argus) based on a habituation paradigm. Chem. Senses 13:385–395.

    Google Scholar 

  • Daviss, B. 2005. Growing pains for metabolomics. Scientist 19:25–28.

    Google Scholar 

  • Derby, C. D. 2000. Learning from spiny lobsters about chemosensory coding of mixtures. Physiol. Behav 69:203–209.

    PubMed  CAS  Google Scholar 

  • Derby, C. D., and Atema, J. 1980. Induced host odor attraction in the pea crab Pinnotheres maculatus. Biol. Bull 158:26–33.

    Google Scholar 

  • Derby, C. D., and Atema, J. 1982. The function of chemo- and mechanoreceptors in lobster (Homarus americanus) feeding behaviour. J. Exp. Biol 98:317–327.

    Google Scholar 

  • Derby, C. D., and Atema, J. 1988. Chemoreceptor cells in aquatic invertebrates: peripheral mechanisms of chemical signal processing in decapod crustaceans, pp. 365–385, in J. Atema, R. R. Fay, A. N. Popper, and W. N. Tavolga (eds.). Sensory Biology of Aquatic Animals. Springer, New York.

    Google Scholar 

  • Derby, C. D., Steullet, P., Horner, A. J., and Cate, H. S. 2001. The sensory basis to feeding behavior in the Caribbean spiny lobster Panulirus argus. Mar. Freshw. Res 52:339–1350.

    Google Scholar 

  • Derby, C. D., Kicklighter, C. E., Johnson, P. M., and Zhang, X. 2007. Chemical composition of inks of diverse marine molluscs suggests convergent chemical defenses. J. Chem. Ecol 33:1105–1113.

    PubMed  CAS  Google Scholar 

  • Dittman, A. D., Quinn, T. P., and Nevitt, G. A. 1996. Timing of imprinting to natural and artificial odors by coho salmon (Oncorhynchus kisutch). Can. J. Fish Aquat. Sci 53:434–442.

    Google Scholar 

  • Dodson, J. J., and Bitterman, M. E. 1989. Compound uniqueness and the interactive role of morpholine in fish chemoreception. Biol. Behav 14:13–27.

    Google Scholar 

  • Døving, K. B., Selset, R., and Thommesen, G. 1980. Olfactory sensitivity to bile acids in salmonid fishes. Acta Physiol. Scand 108:123–131.

    PubMed  Google Scholar 

  • Døving, K. B., Hamdani, E. H., Hoglund, E., Kasumyan, A., and Tuvikene, A. O. 2005. Review of the chemical and physiological basis of alarm reactions in cyprinids, pp. 131–163, in G. von der Emde, J. Mogdans, and B. G. Kapoor (eds.). Senses of Fish. Narosa, New Delhi.

    Google Scholar 

  • Dreanno, C., Matsumura, K., Dohmae, N., Takio, K., Hirota, H., Kirby, R. R., and Clare, A. S. 2006a. An a2-macroglobulin-like protein is the cue to gregarious settlement of the barnacle Balanus amphitrite. Proc. Natl. Acad. Sci. U.S.A 103:14396–14401.

    PubMed  CAS  Google Scholar 

  • Dreanno, C., Kirby, R. R., and Clare, A. S. 2006b. Smelly feet are not always a bad thing: the relationship between cyprid footprint protein and the barnacle settlement pheromone. Biol. Lett 2:423–425.

    PubMed  CAS  Google Scholar 

  • Eisthen, H. L. 2002. Why are olfactory systems of different animals so similar? Brain Behav. Evol 59:273–293.

    PubMed  Google Scholar 

  • Ekerholm, M., and Hallberg, E. 2005. Primer and short-range releaser pheromone properties of pre-moult female urine from the shore crab Carcinus maenas. J. Chem. Ecol 31:1845–1864.

    PubMed  CAS  Google Scholar 

  • Fine, J. M., Vrieze, L. A., and Sorensen, P. W. 2004. Evidence that petromyzontid lampreys employ a common migratory pheromone that is partially comprised of bile acids. J. Chem. Ecol 30:2091–2110.

    PubMed  CAS  Google Scholar 

  • Fine-levy, J. B., Girardot, M.-N., Derby, C. D., and Daniel, P. C. 1988. Differential associative conditioning and olfactory discrimination in the spiny lobster Panulirus argus. Behav. Neural Biol 49:15–331.

    Google Scholar 

  • Finger, T. A. 2008. Sorting food from stones: the vagal taste system in goldfish Carassius auratus. J. Comp. Physiol. A 194:135–143.

    Google Scholar 

  • Finger, T. A., and Morita, Y. 1985. Two gustatory system: facial and vagal gustatory nuclei have different brainstem connections. Science 227:776–778.

    PubMed  CAS  Google Scholar 

  • Friedrich, R. W., and Korsching, S. I. 1998. Chemotopic, combinatorial, and noncombinatorial odorant representations in the olfactory bulb revealed using a voltage-sensitive axon tracer. J. Neurosci 18:9977–9900.

    PubMed  CAS  Google Scholar 

  • Garm, A., and Høeg, J. T. 2006. Ultrastructure and functional organization of mouthpart sensory setae of the spiny lobster Panulirus argus: new features of putative mechanoreceptors. J. Morphol 267:464–476.

    PubMed  Google Scholar 

  • Garm, A., Shabani, S., Høeg, J. T., and Derby, C. D. 2005. Chemosensory neurons in the mouthparts of the spiny lobsters Panulirus argus and Panulirus interruptus (Crustacea: Decapoda). J. Exp. Mar. Biol. Ecol 314:175–186.

    Google Scholar 

  • Gherardi, F., Tricarico, E., and Atema, J. 2005. Unraveling the nature of individual recognition by odor in hermit crabs. J. Chem. Ecol 31:2877–2896.

    PubMed  CAS  Google Scholar 

  • Gleeson, R. A. 1982. Morphological and behavioral identification of the sensory structures mediating pheromone reception in the blue crab Callinectes sapidus. Biol. Bull 163:162–171.

    Google Scholar 

  • Gleeson, R. A. 1991. Intrinsic factors mediating pheromone communication in the blue crab, Callinectes sapidus, pp. 17–32, in R. T. Bauer, and J. W. Martin (eds.). Crustacean Sexual Biology. Columbia University Press, New York.

    Google Scholar 

  • Grasso, F. W., and Basil, J. A. 2002. How lobsters, crayfishes, and crabs locate sources of odor: current perspectives and future directions. Curr. Opin. Neurobiol 12:721–727.

    PubMed  CAS  Google Scholar 

  • Grove, M. W., and Woodin, S. A. 1996. Conspecific recognition and host choice in a pea crab, Pinnixa chaetopterana (Brachyura: Pinnotheridae). Biol. Bull 190:359–366.

    Google Scholar 

  • Gunning, G. E. 1959. The sensory basis of homing in the longear sunfish, Lepomis megalotis megalotis (Rafinsque). Invest. Indiana Lakes Streams 5:103–130.

    Google Scholar 

  • Hamdani, E. H., Stabell, O. B., Alexander, G., and Døving, K. B. 2000. Alarm reaction in the crucian carp is mediated by the medial bundle of the medial olfactory tract. Chem. Senses 25:103–109.

    PubMed  CAS  Google Scholar 

  • Hamdani, E. H., Alexander, G., and Døving, K. B. 2001. Projection of sensory neurons with microvilli to the lateral olfactory tract indicates their participation in feeding behaviour in the crucian carp. Chem. Senses 26:1134–1144.

    Google Scholar 

  • Hanson, L. H. 2001. Coding of pheromonal information in the goldfish olfactory bulb. Ph.D. dissertation, University of Minnesota.

  • Hara, T. J. 1970. An electrophysiological basis for olfactory discrimination in homing salmon: a review. J. Fish. Res. Board Can 27:565–586.

    Google Scholar 

  • Hara, T. J. 1994. The diversity of chemical stimulation in fish olfaction and gustation. Rev. Fish Biol. Fish. 4:1–35.

    Google Scholar 

  • Hara, T. J. 2007. Gustation, pp. 45–96, in T. J. B. S. HaraZielinski (ed.). Fish Physiology Series (A. P. Farrell and C. J. Brauner, eds.). Sensory Systems Neuroscience. Elsevier, New York.

    Google Scholar 

  • Hara, T. J., Macdonald, S., Evans, R. E., Marui, T., and Arai, S. 1984. Morpholine, bile acids, and skin mucous as possible chemical cues in salmonid homing: electrophysiological re-evaluation, pp. 363–378, in J. D. McCleave, G. P. Arnold, J. J. Dodson, and W. Neill (eds.). Mechanisms of Migration in Fishes. Plenum, New York.

    Google Scholar 

  • Hardege, J. D., Jennings, A., Hayden, D., Muller, C. T., Pascoe, D., Bentley, M. G., and Clare, A. S. 2002. Novel behavioural assay and partial purification of a female-derived sex pheromone in Carcinus maenas. Mar. Ecol. Prog. Ser 244:179–189.

    CAS  Google Scholar 

  • Hasler, A. D., and Wisby, W. J. 1951. Discrimination of stream odors by fishes and relation to parent stream behavior. Am. Nat 85:223–238.

    CAS  Google Scholar 

  • Hasler, A. D., and Scholz, A. T. 1983. Olfactory Imprinting and Homing in Salmon. Investigations in the Mechanism of the Imprinting Process. p. 134. Springer, Berlin.

    Google Scholar 

  • Hay, M. E. 1996. Marine chemical ecology: what’s known and what’s next? J. Exp. Mar. Biol. Ecol 200:103–134.

    CAS  Google Scholar 

  • Hayden, D., Jennings, A., Müller, C., Pascoe, D., Bublitz, R., Webb, H., Breithaupt, T., Watkins, L., and Hardege, J. 2007. Sex-specific mediation of foraging in the shore crab, Carcinus maenas. Horm. Behav 52:162–168.

    PubMed  CAS  Google Scholar 

  • Hazlett, B. A. 1994. Alarm responses in the crayfish Orconectes virilis and Orconectes propinquus. J. Chem. Ecol 20:1525–1535.

    Google Scholar 

  • Hazlett, B. A. 2003. Predator recognition and learned irrelevance in the crayfish Orconectes virilis. Ethology 109:765–780.

    Google Scholar 

  • Hildebrand, J. G., and Shepherd, G. M. 1997. Mechanisms of olfactory discrimination: converging evidence for common principals across phyla. Annu. Rev. Neurosci 20:595–561.

    PubMed  CAS  Google Scholar 

  • Holland, K. M., and Teeter, J. H. 1981. Behavioral and cardiac reflex assays of the chemosensory acuity of channel catfish to amino acids. Physiol. Behav 27:699–707.

    PubMed  CAS  Google Scholar 

  • Horner, A. J., Weissburg, M. J., and Derby, C. D. 2004. Dual chemosensory pathways can mediate orientation of spiny lobsters to distant food odors. J. Exp. Biol 207:3785–3796.

    PubMed  Google Scholar 

  • Horner, A. J., Nickles, S. P., Weissburg, M. J., and Derby, C. D. 2006. Source and specificity of chemical cues mediating shelter preference of Caribbean spiny lobsters (Panulirus argus). Biol. Bull 211:128–139.

    PubMed  Google Scholar 

  • Horner, A. J., Schmidt, M., Edwards, D. H., and Derby, C. D. 2008a. Role of the olfactory pathway in agonistic behavior of crayfish Procambarus clarkii. Invertebr. Neurosci 8:11–18.

    Google Scholar 

  • Horner, A. J., Weissburg, M. J., and Derby, C. D. 2008b. The olfactory pathway mediates sheltering behavior of Caribbean spiny lobsters, Panulirus argus, to conspecific urine signals. J. Comp. Physiol. A 194:243–253.

    Google Scholar 

  • Ishimaru, Y., Okada, S., Naito, H., Nagai, T., Yasuoka, A., Matsumoto, I., and Abe, K. 2005. Two families of candidate taste receptors in fishes. Mech. Dev 122:1310–1321.

    PubMed  CAS  Google Scholar 

  • Johnson, M. E., and Atema, J. 2005. The olfactory pathway for individual recognition in the American lobster Homarus americanus. J. Exp. Biol 208:2865–2872.

    PubMed  Google Scholar 

  • Jones, K. A. 1992. Food search and behaviour in fish and the use of chemical lures in commercial and sports fishing, pp. 288–320, in T. J. Hara (ed.). Fish Chemoreception. Chapman and Hall, New York.

    Google Scholar 

  • Kamio, M., Matsunaga, S., and Fusetani, N. 2002. Copulation pheromone in the crab Telmessus cheiragonus (Brachyura: Decapoda). Mar. Ecol. Prog. Ser 234:183–190.

    Google Scholar 

  • Kamio, M., Kubanek, J., and Derby, C. 2006. N-Acetylglucosamino-1,5-lactone is a candidate sex pheromone in female blue crabs. Chem. Senses 31:A82.

    Google Scholar 

  • Kamio, M., Kicklighter, C., Ko, K.-C., Nusnbaum, M., Aggio, J., Hutchins, M., and Derby, C. 2007. Defense through chemoreception: an l-amino acid oxidase in the ink of sea hares deters predators through their chemical senses. Chem. Senses 32:A37.

    Google Scholar 

  • Kamio, M., Reidenbach, M. A., and Derby, C. D. 2008. To paddle or not: context dependent courtship display by male blue crabs, Callinectes sapidus. J. Exp. Biol 211:1243–1248.

    PubMed  Google Scholar 

  • Kapoor, B. G., and Finger, T. E. 2003. Taste and solitary chemoreceptor cells, pp. 753–769, in G. Arratia, B. G. Kapoor, M. Chardon, and R. Diogo (eds.). Catfishes, vol. 2. Science, Enfield, New Hampshire.

    Google Scholar 

  • Karavanich, C., and Atema, J. 1998. Individual recognition and memory in lobster dominance. Anim. Behav 56:1553–1560.

    PubMed  Google Scholar 

  • Keller, T. A., and Weissburg, M. J. 2004. Effects of odor flux and pulse rate on chemosensory tracking in turbulent odor plumes by the blue crab, Callinectes sapidus. Biol. Bull 207:44–55.

    PubMed  Google Scholar 

  • Kicklighter, C. E., Shabani, S., Johnson, P. M., and Derby, C. D. 2005. Sea hares use novel antipredatory chemical defenses. Curr. Biol 15:549–554.

    PubMed  CAS  Google Scholar 

  • Kobayashi, M., Sorensen, P. W., and Stacey, N. E. 2002. Hormonal and pheromonal control of spawning in goldfish. Fish Physiol. Biochem 26:71–84.

    CAS  Google Scholar 

  • Krasne, F. B. 1973. Learning in Crustacea, pp. 49–130, in W. C. Corning, J. A. Dyal, and A. O. D. Willows (eds.). Invertebrate Learning. Vol. 2: Arthropods and Gastropod Mollusks. Plenum, New York.

    Google Scholar 

  • Kupchan, S. M., Britton, R. W., Lacadie, J. A., Ziegler, M. F., and Sigel, C. W. 1975. The isolation and structural elucidation of bruceantin and cruceantinol. J. Org. Chem 40:648–654.

    PubMed  CAS  Google Scholar 

  • Lane, A. L., and Kubanek, J. 2006. Structure–activity relationship of chemical defenses from the freshwater plant Micranthemum umbrosum. Phytochemistry 67:1224–1231.

    PubMed  CAS  Google Scholar 

  • Li, W., Scott, A. P., Siefkas, M. J., Yan, H., Liu, Q., Yun, S.-S., and Gage, D. A. 2002. Bile acid secreted by male sea lamprey that acts as sex pheromone. Science 296:138–141.

    PubMed  CAS  Google Scholar 

  • Little, E. E. 1975. Chemical communication in maternal behaviour of crayfish. Nature 255:400–401.

    PubMed  CAS  Google Scholar 

  • Little, E. E. 1976. Ontogeny of maternal behavior and brood pheromone in crayfish. J. Comp. Physiol. A 112:133–142.

    Google Scholar 

  • Little, E. E. 1977. Conditioned aversion to amino acid flavors in the catfish, Ictalurus punctatus. Physiol. Behav 19:743–747.

    PubMed  CAS  Google Scholar 

  • Luu, P., Achner, F., Bertrand, H.-O., Fan, J., and Ngai, J. 2004. Molecular determinants of ligand selectivity in a vertebrate odorant receptor. J. Neurosci 24:10128–10137.

    PubMed  CAS  Google Scholar 

  • Mackie, A. M. 1982. Identification of the gustatory feeding stimulants, pp. 275–291, in T. J. Hara (ed.). Chemoreception in Fishes. Elsevier, New York.

    Google Scholar 

  • Maniak, P. J., Lossing, R., and Sorensen, P. W. 2000. Injured Eurasian ruffe, Gymnocephalus cernuss, release an alarm pheromone which may prove useful in their control. J. Great Lakes Res 26:183–195.

    Google Scholar 

  • Mcclintock, T. S., Ache, B. W., and Derby, C. D. 2006. Lobster olfactory genomics. Integr. Comp. Biol 46:940–947.

    CAS  Google Scholar 

  • Michel, W. C. 2006. Chemoreception, pp. 471–497, in D. H. Evans, and J. B. Claiborne (eds.). The Physiology of Fishes. 3rd edn.CRC, Boca Raton, FL.

    Google Scholar 

  • Moore, P. A. 2007. Agonistic behavior in freshwater crayfish: the influence of intrinsic and extrinsic factors on aggressive behavior and dominance, pp. 90–114, in J. E. Duffy, and M. Thiel (eds.). Evolutionary Ecology of Social and Sexual Systems: Crustacea as Model Organisms. Oxford University Press, Oxford, UK.

    Google Scholar 

  • Moore, P. A., and Bergman, D. A. 2005. The smell of success and failure: the role of intrinsic and extrinsic chemical signals on the social behavior of crayfish. Integr. Comp. Biol 45:650–657.

    CAS  Google Scholar 

  • Moyle, P. B., and Cech, J. J. 2000. Fishes: An Introduction to Ichthyology. 3rd edn.Prentice Hall, New York.

    Google Scholar 

  • Nevitt, G., Pentcheff, N. D., Lohmann, K. J., and Zimmer, R. K. 2000. Den selection by the spiny lobster Panulirus argus: testing attraction to conspecific odors in the field. Mar. Ecol. Prog. Ser 203:225–231.

    Google Scholar 

  • Nevitt, G. A., Dittman, A. D., Quinn, T. P., and Moody, W. J. 2004. Evidence for a peripheral olfactory memory in imprinted salmon. Proc. Nat Acad. Sci. U.S.A. 91:4288–4292.

    Google Scholar 

  • Ngai, J., Dowling, M. M., Buck, L., Axel, R., and Chess, A. 1993. The family of genes encoding odorant receptors in the channel catfish. Cell 72:657–666.

    PubMed  CAS  Google Scholar 

  • Nikonov, A. A., and Caprio, J. 2001. Electrophysiological evidence for a chemotopy of naturally relevant odors in the channel catfish. J. Neurophysiol 86:1869–1876.

    PubMed  CAS  Google Scholar 

  • Nikonov, A. A., Finger, T. A., and Caprio, J. 2005. Beyond the olfactory bulb: an odotopic map in the forebrain. Proc. Natl. Acad. Sci. U.S.A 102:18688–18693.

    PubMed  CAS  Google Scholar 

  • Nordeng, H. 1977. A pheromone hypothesis for homeward migration in anadromous salmonids. Nature 233:411–413.

    Google Scholar 

  • Oike, H., Nagai, T., Furuyama, A., Okada, S., Aihara, Y., Ishimaru, Y., Marui, T., Matsumoto, I., Misaka, T., and Abe, K. 2007. Characterization of ligands for fish taste receptors. J. Neurosci 27:5584–5592.

    PubMed  CAS  Google Scholar 

  • Parker, J. D., Burkepile, D. E., Collins, D. O., Kubanek, J., and Hay, M. E. 2007. Stream mosses as chemically-defended refugia for freshwater macroinvertebrates. Oikos 116:302–312.

    CAS  Google Scholar 

  • Pfeiffer, W., Riegelbauer, G., Meier, G., and Scheibler, B. 1985. Effect of hypoxanthine-3-N-oxide on central nervous excitation of the black tetra, Gymnocorymbus ternetzi (Characidae, Ostariophysi, Pisces) indicated by dorsal light response. J. Chem. Ecol 11:507–523.

    CAS  Google Scholar 

  • Poling, K. R., Fraser, E. J., and Sorensen, P. W. 2001. The three steroidal components of the goldfish preovulatory pheromone signal evoke different behaviors in males. Comp. Biochem. Physiol 129B:645–651.

    CAS  Google Scholar 

  • Prusak, A. C., O’neal, J., and Kubanek, J. 2005. Prevalence of chemical defenses among freshwater plants. J. Chem. Ecol 31:1145–1160.

    PubMed  CAS  Google Scholar 

  • Reusch, T. B., Haberli, M. A., Aeschlimann, P. B., and Milinski, M. 2002. Female sticklebacks in a strategy of sexual selection explaining MHC polymorphism. Nature 414:300–302.

    Google Scholar 

  • Rittschof, D., and Cohen, J. H. 2004. Crustacean peptide and peptide-like pheromones and kairomones. Peptides 25:1503–1516.

    PubMed  CAS  Google Scholar 

  • Rittschof, D., Tsai, D. W., Massey, P. G., Blanco, L., Kueber, G. L., and Haas, R. J. 1992. Chemical mediation of behavior in hermit crabs: alarm and aggregation cues. J. Chem. Ecol 18:959–984.

    Google Scholar 

  • Robertson, J. R., Fudge, J. A., and Vermeer, G. K. 1981. Chemical and live feeding stimulants of the sand fiddler crab, Uca pugilator (Bose). J. Exp. Mar. Biol. Ecol 53:47–64.

    CAS  Google Scholar 

  • Rolen, S. H., Sorensen, P. W., Mattson, D., and Caprio, J. 2003. Polyamines as olfactory stimuli in the goldfish, Carassius auratus. J. Exp. Biol 206:1683–1696.

    PubMed  CAS  Google Scholar 

  • Saraiva, L. R., and Korsching, S. I. 2007. A novel olfactory receptor gene family in teleost fish. Genome Res 17:1448–1457.

    PubMed  CAS  Google Scholar 

  • Schachtner, J., Schmidt, M., and Homberg, U. 2005. Organization and evolutionary trends of primary olfactory brain centers in Tetraconata (Crustacea plus Hexapoda). Arthropod. Struct. Dev 34:257–299.

    Google Scholar 

  • Schaefer, M. L., Young, D. A., and Restrepo, D. 2001. Olfactory fingerprints for major histocompatibility body odors. J. Neurosci 21:2481–2487.

    PubMed  CAS  Google Scholar 

  • Schmidt, M., and Derby, C. D. 2005. Non-olfactory chemoreceptors in asymmetric setae activate antennular grooming behavior in the Caribbean spiny lobster Panulirus argus. J. Exp. Biol 208:233–248.

    PubMed  CAS  Google Scholar 

  • Shabani, S., Kamio, M., and Derby, C. D. 2006. Chemicals released by injured or disturbed conspecifics mediate defensive behaviors via the aesthetasc pathway in the spiny lobster Panulirus argus. Chem. Senses 31:A81–A82.

    Google Scholar 

  • Shoji, T., Yamamoto, Y., Nishikawa, D., Kurihara, K., and Ueda, H. 2003. Amino acids in stream waters are essential for salmon homing migration. Fish Physiol. Biochem 28:249–251.

    CAS  Google Scholar 

  • Shuranova, Z., Burmistrov, Y., and Abramson, C. I. 2005. Habituation to a novel environment in the crayfish (Procambarus cubensis). J. Crustac. Biol 25:488–494.

    Google Scholar 

  • Smith, R. J. F. 1992. Alarm signals in fish. Rev. Fish Biol. Fish 2:33–63.

    Google Scholar 

  • Sorensen, P. W. 2007. Goldfish can be conditioned to respond to a sex pheromone. Chem. Senses 32:A19.

    Google Scholar 

  • Sorensen, P. W., and Scott, A. P. 1994. The evolution of hormonal sex pheromones in teleost fish: poor correlation between the pattern of steroid release by goldfish and olfactory sensitivity suggests that these cues evolved as a result of chemical spying rather than signal specialization. Acta Scand. Physiol 152:191–205.

    CAS  Google Scholar 

  • Sorensen, P. W., and Caprio, J. 1998. Chemoreception in fish, pp. 375–406, in R. E. Evans (ed.). The Physiology of Fishes. 2nd edn.CRC, Florida.

    Google Scholar 

  • Sorensen, P. W., and Stacey, N. E. 1999. Evolution and specialization in fish hormonal pheromones, pp. 15–48, in R. E. Johnston, D. Müller-Schwarze, and P. W. Sorensen (eds.). Advances in Chemical Signals in Vertebrates. Plenum, New York.

    Google Scholar 

  • Sorensen, P. W., and Sato, K. 2005. Second messenger systems mediating sex pheromone and amino acid sensitivity in goldfish olfactory receptor neurons. Chem. Senses 30:Suppl. 1315–316.

    Google Scholar 

  • Sorensen, P. W., and Hoye, T. R. 2007. A critical review of the discovery and application of a migratory pheromone in an invasive fish, the sea lamprey Petromyzon marinus L. J. Fish Biol 71:100–114.

    CAS  Google Scholar 

  • Sorensen, P. W., Hara, T. J., Stacey, N. E., and Goetz, F. W. 1988. F prostaglandins function as potent olfactory stimulants that comprise the postovulatory female sex pheromone in goldfish. Biol. Reprod. 39:1039–1050.

    PubMed  CAS  Google Scholar 

  • Sorensen, P. W., Hara, T. J., Stacey, N. E., and Dulka, J. G. 1990. Extreme olfactory specificity of male goldfish to the preovulatory pheromone 17a,20b-dihydroxy-4-pregnen-3-one. J. Comp. Physiol. A 166:373–385.

    Google Scholar 

  • Sorensen, P. W., Hara, T. J., and Stacey, N. E. 1991. Sex pheromones selectively stimulate the medial olfactory tracts of male goldfish. Brain Res 558:343–347.

    PubMed  CAS  Google Scholar 

  • Sorensen, P. W., Scott, A. P., Stacey, N. E., and Bowdin, L. 1995. Sulfated 17,20b-dihydroxy-4-pregnen-3-one functions as a potent and specific olfactory stimulant with pheromonal actions in the goldfish. Gen. Comp. Endocrinol 100:128–142.

    PubMed  CAS  Google Scholar 

  • Sorensen, P. W., Scott, A. P., and Kihslinger, R. L. 2000. How common hormonal metabolites function as specific pheromones in the goldfish, pp. 125–129, in B. Norberg, O. S. Kjesbu, G. L. Taranger, E. Andersson, and S. O. Stefansson (eds.). Proceedings of the Sixth International Symposium on the Reproductive Physiology of Fish. Bergen, Norway.

  • Sorensen, P. W., Vrieze, L. A., and Fine, J. 2003. A multicomponent migratory pheromone in the sea lamprey. Fish Physiol. Biochem 28:253–257.

    CAS  Google Scholar 

  • Sorensen, P. W., Fine, J. M., Dvornikovs, V., Jeffrey, C. S., Shao, F., Wang, J., Vrieze, L. A., Anderson, K. R., and Hoye, T. R. 2005. Mixture of new sulfated steroids functions as a migratory pheromone in the sea lamprey. Nat. Chem. Biol 1:324–328.

    PubMed  CAS  Google Scholar 

  • Stacey, N. E., and Kyle, A. L. 1983. Effects of olfactory tract lesions on sexual and feeding behavior in the goldfish. Physiol. Behav 30:621–628.

    PubMed  CAS  Google Scholar 

  • Stacey, N. E., and Sorensen, P. W. 2005. Hormones, pheromones, and reproductive behaviors, pp. 359–412, in K. A. Sloman, S. Balshine, and R. W. Wilson (eds.). Behaviour: Interactions with Fish Physiology, vol. 24 in Fish Physiology (W. S. Hoar, D. J. Randall, and A. P. Farrell, series eds.). Academic, New York.

    Google Scholar 

  • Stebbing, P. D., Bentley, M. G., and Watson, G. J. 2003. Mating behaviour and evidence for a female released courtship pheromone in the signal crayfish Pacifastacus leniusculus. J. Chem. Ecol 29:465–475.

    PubMed  CAS  Google Scholar 

  • Steullet, P., and Derby, C. D. 1997. Coding of blend ratios of binary mixtures by olfactory neurons in the Florida spiny lobster, Panulirus argus. J. Comp. Physiol. A 180:123–135.

    PubMed  CAS  Google Scholar 

  • Steullet, P., Dudar, O., Flavus, T., Zhou, M., and Derby, C. D. 2001. Selective ablation of antennular sensilla on the Caribbean spiny lobster Panulirus argus suggests that dual antennular chemosensory pathways mediate odorant activation of searching and localization of food. J. Exp. Biol 204:4259–4269.

    PubMed  CAS  Google Scholar 

  • Steullet, P., Kruetzfeldt, D. R., Hamidani, G., Flavus, T., Ngo, V., and Derby, C. D. 2002. Dual parallel antennular chemosensory pathways mediate odor-associative learning and odor discrimination in the Caribbean spiny lobster Panulirus argus. J. Exp. Biol 205:851–867.

    PubMed  Google Scholar 

  • Tankersley, R. A., Bullock, T. M., Forward, R. B., and Rittschof, D. 2002. Larval release behaviors in the blue crab Callinectes sapidus: role of chemical cues. J. Exp. Mar. Biol. Ecol 273:1–14.

    CAS  Google Scholar 

  • Ting, J. H., and Snell, T. W. 2003. Purification and sequencing of a mate-recognition protein from the copepod Tigriopus japonicus. Mar. Biol 143:1–8.

    CAS  Google Scholar 

  • Trott, T. J., and Robertson, J. R. 1984. Chemical stimulants of cheliped flexion behavior by the western Atlantic ghost crab Ocypode quadrata (Fabricius). J. Exp. Mar. Biol. Ecol 78:237–252.

    CAS  Google Scholar 

  • Valentinčič, T. 2005. Taste and olfactory stimuli and behavior in fishes, pp. 65–85, in G. von der Emde, J. Mogdans, and B. G. Kapoor (eds.). Senses of FishNarosa, New Delhi.

    Google Scholar 

  • Valentinčič, T. S., and Caprio, J. C. 1994. Consummatory behavior in intact and anosmic channel catfish Ictalurus punctatus to amino acids. Physiol. Behav 55:857–863.

    PubMed  Google Scholar 

  • Valentinčič, T. S., and Caprio, J. C. 1997. Visual and chemical release of feeding behavior in adult rainbow trout. Chem. Senses 22:375–382.

    PubMed  Google Scholar 

  • Valentinčič, T. S., Kralj, M., Stenovec, A., and Caprio, J. C. 2000. The behavioral detection of binary mixtures of amino acids and their individual components by catfish. J. Exp. Biol 203:3307–3317.

    PubMed  Google Scholar 

  • Voigt, R., and Atema, J. 1992. Tuning of chemoreceptor cells of the second antenna of the American lobster (Homarus americanus) with a comparison of four of its other chemoreceptor organs. J. Comp. Physiol. A 171:673–683.

    Google Scholar 

  • Von frisch, K. 1938. Zur Psychologie des Fisch-schwarmes. Naturwissenschaften 226:601–606.

    Google Scholar 

  • Ward, A. J. W., and Hart, P. J. B. 2002. The effects of kin and familiarity on interactions between fish. Fish & Fisheries 4:348–358.

    Google Scholar 

  • Weissburg, M. J., and Zimmer-faust, R. K. 1991. Ontogeny versus phylogeny in determining patterns of chemoreception: initial studies with fiddler crabs. Biol. Bull 181:205–215.

    CAS  Google Scholar 

  • Weissburg, M. J., Ferner, M. C., Pisut, D. P., and Smee, D. L. 2002. The ecology of chemically-mediated prey perception. J. Chem. Ecol 28:1933–1950.

    Google Scholar 

  • Wight, K., Francis, L., and Eldridge, D. 1990. Food aversion learning by the hermit crab Pagurus granosimanus. Biol. Bull 178:205–209.

    Google Scholar 

  • Wisenden, B. D. 2000. Olfactory assessment of predation risk in the aquatic environment. Phil. Trans R. Soc. Lond. B 355:1205–1208.

    CAS  Google Scholar 

  • Wong, B. B. M., Fisher, H. S., and Rosenthal, G. G. 2005. Species recognition of male swordtails by chemical cues. Behav. Ecol 16:818–821.

    Google Scholar 

  • Yambe, Y., Kitamura, S., Kamio, M., Yamada, M., Matsunaga, M., Fusetani, N., and Yamazaki, F. 2007. l-Kynurenine, an amino acid identified as a sex pheromone in the urine of ovulated female masu salmon. Proc. Nat. Acad. Sci. U.S.A 103:15370–15374.

    Google Scholar 

  • Zimmer, R. K., and Butman, C. A. 2000. Chemical signaling processes in the marine environment. Biol. Bull 198:168–187.

    PubMed  CAS  Google Scholar 

  • Zimmer, R. K., and Derby, C. D. 2007. Biological Bulletin virtual symposium: the neuroecology of chemical defense. Biol. Bull 213:205–207.

    PubMed  Article  Google Scholar 

  • Zimmer, R. K., and Zimmer, C. A. 2008. Dynamic scaling in chemical ecology. J. Chem. Ecol. this issue

  • Zimmer-faust, R. K. 1993. ATP: a potent prey attractant evoking carnivory. Limnol. Oceanogr 38:1271–1275.

    CAS  Article  Google Scholar 

  • Zimmer-faust, R. K., and Case, J. F. 1982a. Odors influencing foraging behavior of the California spiny lobster, Panulirus interruptus, and other decapod Crustacea. Mar. Behav. Physiol 9:35–58.

    Article  Google Scholar 

  • Zimmer-faust, R. K., and Case, J. F. 1982b. Organization of food search in the kelp crab, Pugettia producta (Randall). J. Exp. Mar. Biol. Ecol 57:237–255.

    Google Scholar 

  • Zimmer-faust, R. K., Tyre, J. E., and Case, J. F. 1985. Chemical attraction causing aggregation in the spiny lobster, Panulirus interruptus (Randall), and its probable ecological significance. Biol. Bull 169:106–118.

    Google Scholar 

  • Zippel, H. P., Voigt, R., Knaust, M., and Luan, Y. 1993. Spontaneous behaviour, training, and discrimination training in goldfish using chemosensory stimuli. J. Comp. Physiol. A 172:81–90.

    Google Scholar 

  • Zulandt schneider, R. A., and Moore, P. A. 2000. Urine as a source of conspecific disturbance signals in the crayfish Procambarus clarkii. J. Exp. Biol 203:765–771.

    PubMed  CAS  Google Scholar 

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Acknowledgment

We thank our many colleagues who have contributed to work in this field. We also thank our current funding sources for support during preparation of this review (NIH DC00312, NSF IBN-0614685, Legislative Citizen Commission for Minnesota Resources, and the Minnesota Agriculture Experiment Station).

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  1. Brains and Behavior Program, Center for Behavioral Neuroscience, Department of Biology, Georgia State University, Atlanta, GA, USA

    Charles D. Derby

  2. Department of Fisheries and Wildlife, University of Minnesota, St. Paul, MN, USA

    Peter W. Sorensen

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Correspondence to Charles D. Derby.

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Derby, C.D., Sorensen, P.W. Neural Processing, Perception, and Behavioral Responses to Natural Chemical Stimuli by Fish and Crustaceans. J Chem Ecol 34, 898–914 (2008). https://doi.org/10.1007/s10886-008-9489-0

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Keywords

  • Chemical ecology
  • Chemoreception
  • Gustation
  • Olfaction
  • Pheromone