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Journal of Chemical Ecology

, Volume 28, Issue 10, pp 1953–1970 | Cite as

Ecological Consequences of Chemically Mediated Prey Perception

  • Marc J. Weissburg
  • Matthew C. Ferner
  • Daniel P. Pisut
  • Delbert L. Smee
Article

Abstract

To locate food, mobile consumers in aquatic habitats perceive and move towards sources of attractive chemicals. There has been much progress in understanding how consumers use chemicals to identify and locate prey despite the elusive identity of odor signals and the complex effects of turbulence on chemical dispersion. This review highlights how integrative studies on behavior, fluid physics, and chemical isolation can be fundamental in elucidating mechanisms that regulate species composition and distribution. We suggest three areas where further research may yield important ecological insights. First, although basic aspects of stimulatory molecules are known, our understanding of how consumers identify prey from a distance remains poor, and the lack of studies examining the influence of distance perception on food preference may result in inaccurate estimation of foraging behavior in the field. Second, the ability of many animals to find prey is greatest in unidirectional, low turbulence flow environments, although recent evidence indicates a trade-off in movement speed versus tracking ability in turbulent conditions. This suggests that predator foraging mode may affect competitive interactions among consumers, and that turbulence provides a hydrodynamic refuge in space or time, leading to particular associations between predator success, prey distributions, and flow. Third, studies have been biased towards examining predator tracking. Current data suggest a variety of mechanisms prey may use to disguise their presence and avoid predation; these mechanisms also may produce associations between prey and flow environments. These examples of how chemical attraction may mediate interactions between consumers and their resources suggest that the ecology of chemically mediated prey perception may be as fundamental to the organization of aquatic communities as the ecology of chemical deterrence.

Chemical attraction chemosensation community structure flow foraging odor plumes olfaction orientation predator-prey turbulence 

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REFERENCES

  1. Arnold, W. S. 1984. The effects of prey size, predator size and sediment composition on the rate of predation of the blue crab Callinectes sapidus Rathbun on the hard clam Mercenaria mercenaria (Linne). J. Exp. Mar. Biol. Ecol. 80:207–219.Google Scholar
  2. Britton, J. C. and Morton, B. 1994. Marine carrion and scavengers. Oceanogr. Mar. Biol. Annu. Rev. 32:369–434.Google Scholar
  3. Caprio, J., Barnd, J. G., Tetter, J. H., Ventincic, T., Kalinoksi, L., Kohbara, J., Kumazawa, T., and Wegert, S. 1993. The taste system of the channel catfish: from biophysics to behavior. Trends Neurosci. 16:192–197.Google Scholar
  4. Carr, W. E. S. 1978. Chemoreception in the shrimp Palaemonetes pugio: The role of amino acids and betaine in elicitation of a feeding response by extracts. Comp. Biochem. Physiol. 61A:127–131.Google Scholar
  5. 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.). The Sensory Biology of Aquatic Animals. Springer-Verlag, New York.Google Scholar
  6. Carr, W. E. S. and Derby, C. D. 1986a. Behavioral chemoattractants for the shrimp, Palaemontes pugio: identification of active components in food extracts and evidence of synergistic mixture interactions. Chem. Senses 11:49–64.Google Scholar
  7. Carr, W. E. S. and C. D. Derby. 1986b. Chemically stimulated feeding behavior in marine animals: the importance of chemical mixtures and the involvement of mixture interactions. J. Chem. Ecol. 12:989–1011.Google Scholar
  8. Carr, W. E. S., Netherton, J. C., III, Gleeson, R. A., and Derby, C. D. 1996. Stimulants of feeding behavior in fish: analysis of tissues of diverse marine organisms. Biol. Bull. 190:149–160.Google Scholar
  9. Cote, I. M. and Jelnikar, E. 1999. Predator-induced clumping behavior in mussels (Mytilus edulis Linnaeus). J. Exp. Mar. Biol. Ecol. 235:201–211.Google Scholar
  10. Curtis, L. A. and Hurd, L. E. 1985. On the broad nutritional requirements of the mud snail Ilyanassa (Nassarius) obsoleta Say, and its polytrophic role in the food web. J. Exp. Mar. Biol. Ecol. 41:289–297.Google Scholar
  11. 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.). The Sensory Biology of Aquatic Animals. Springer-Verlag.Google Scholar
  12. Devine, D. V. and Atema, J. 1982. Function of chemoreceptor organs in spatial orientation of the lobster, Homarus americanus: differences and overlap. Biol. Bull. 163: 144–153.Google Scholar
  13. Estes, J. A., Tinker, M. T., Williams, T. M., and Doak, D. F. 1998. Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282:473–476.Google Scholar
  14. Finelli, C. M., Pentcheff, N. D., Zimmer, R. K., and Wethey, D. S. 2000. Physical constraints on ecological processes: a field test of odor-mediated foraging. Ecology 81:784–797.Google Scholar
  15. Hamner, P. and Hamner, W.M. 1977. Chemosensory tracking of scent trails by the planktonic shrimp Acetes sibogae australis. Science 195:886–888. 1968 WEISSBURG, FERNER, PISUT, AND SMEEGoogle Scholar
  16. Hay, M. E. 1996. Marine chemical ecology: What's known and what's next? J. Exp. Mar. Biol. Ecol. 200:103–134.Google Scholar
  17. Hay, M. E., Lee, R. R., Guieb, R. A., and Bennett, M. M. 1986. Food preference and chemotaxis in the sea urchin Arbacia punctulata. J. Exp. Mar. Biol. Ecol. 96:147–153.Google Scholar
  18. Hines, A. H., Haddon, A. M., and Wiechert, L. A. 1990. Guild structure and foraging impact of blue crabs and epibenthic fish in a subestuary of Chesapeake Bay. Mar. Ecol. Prog. Sci. 67:105–126.Google Scholar
  19. Kats, L. B. and Dill, L. M. 1998. The scent of death: chemosensory assessment of predation risk by prey animals. Ecoscience 5:361–394.Google Scholar
  20. Klinger, T. S. and Lawrence, J.M. 1985. Distance perception of food and the effect of food quantity on feeding behavior of Lytechinus variegatus (Lamarck) (Echinodermata:Echinoidea). Mar. Behav. Physiol. 11:327–344.Google Scholar
  21. Lapointe, V. and B. Sainte-Marie. 1992. Currents, predators, and the aggregation of the gastropod Buccinum undatum around bait. Mar. Ecol. Prog. Ser. 85:245–257.Google Scholar
  22. Leonard, G. H., Bertness, M. D., and Yund, P. J. 1999. Crab predation, waterborne cues, and inducible defenses in the blue mussel, Mytilus edulis. Ecology 80:1–14.Google Scholar
  23. Mafra-Neto, A. and Carde, R. T. 1994. Fine-scale structure of pheromone plumes modulates upwind orientation of flying moths. Nature 369:142–144.Google Scholar
  24. Mafra-Neto, A. and CardÉ, R. T. 1998. Rate of realized interception on pheromone pulses in different wind speeds modulates almond moth orientation. J. Comp. Physiol. A. 182:563–572.Google Scholar
  25. Manahan, D.T. 1990. Adaptations by marine invertebrate larvae for nutrient acquisition from seawater. Am. Zool. 30:147–160.Google Scholar
  26. Mann, K. H. and Lazier, J. R. N. 1991. Dynamics of Marine Ecosystems: Biological–Physical Interactions in the Oceans. Blackwell Scientific Publications, Cambridge, Massachusetts.Google Scholar
  27. Mann, K. H., Wright, J. L. C., Welsford, B. E., and Hatfield, E. 1984. Responses of sea urchins Strongylocentrotus droebachiensis (O.F. Muller) to water-borne stimuli from potential predators and potential food algae. J. Exp. Mar. Biol. Ecol. 79:233–244.Google Scholar
  28. Mead, K. S. and Koehl, M. A. R. 2000. Stomatopod antennule design: the asymmetry, sampling efficiency and ontogeny of olfactory flicking. J. Exp. Biol. 203:3795–3808.Google Scholar
  29. Micheli, F. 1997. Effects of predator foraging behavior on patterns of prey mortality in marine soft bottoms. Ecol. Monogr. 67:203–224.Google Scholar
  30. Monismith, S. G., Koseff, J. R., Thompson, J. K., O'Riordan, C. A., and Nepf, H. M. 1990. A study of model bivalve siphonal currents. Limnol. Oceanogr. 35:680–696.Google Scholar
  31. Montgomery, J. C., Diebel, C., Halstead, M. B. D., and Downer, J. 1999. Olfactory search tracks in the Antarctic fish, Trematomus bernacchii. Polar Biol. 21:151–154.Google Scholar
  32. Moore, P. A. and Atema, J. 1991. Spatial Information in the 3-dimensional fine-structure of an aquatic odor plume. Biol. Bull. 181:408–418.Google Scholar
  33. Moore, P. A. and Grills, J. L. 1999. Chemical orientation to food by the crayfish, Oronoectes rusticus, influence by hydrodynamics. Anim. Behav. 58:953–963.Google Scholar
  34. Moore, P. A., Weissburg, M. J., Parrish, J. M., Zimmer-Faust, R. K., and Gerhardt, G. A. 1994. Spatial distribution of odors in simulated benthic boundary layer flows. J. Chem. Ecol. 20:255–279.Google Scholar
  35. Moore, P. A., Grills, J. L., and Schneider, R. W. S. 2000. Habitat-specific signal structure for olfaction: an example from artificial streams. J. Chem. Ecol. 26:565–584.Google Scholar
  36. Murlis, J. 1986. The structure of odour plumes, pp. 27–38 in T. L. PPAYNE, M. C. BIRCH, and C. E. J. KENNEDY, (eds.). Mechanisms in Insect Olfaction. Clarendon Press, Oxford.Google Scholar
  37. Nakaoka, M. 2000. Nonlethal effects of predators on prey populations: predator-mediated change in bivalve growth. Ecology 81:1031–1045.Google Scholar
  38. Person, W. and Olla, B. 1977. Chemoreception in the blue crab. Callinectes sapidus. Biol. Bull. 153:346–354. CHEMICALLY-MEDIATED PREY PERCEPTION 1969Google Scholar
  39. Pennings, S. C. and Bertness, M.D. 2001. Salt marsh communities, pp. 131–157 in M. D. BERTNESS, S. D. GAINES, and M. E. HAY, (eds.). Marine Community Ecology. Sinauer Associates, Sunderland, Massachusetts.Google Scholar
  40. Rahman, Y. J., Forward, R. B., and Rittschof, D. 2000. Responses of mud snails and periwinkles to environmental odors and disaccharide mimics of fish odor. J. Chem. Ecol. 26:679–696.Google Scholar
  41. Reeder, P. B. and Ache, B.W. 1980. Chemotaxis in the Florida spiny lobster, Panulirus argus. Anim. Behav. 28:831–839.Google Scholar
  42. Rittschof, D. 1990. Peptide-mediated behaviors in marine organisms-evidence for a common theme. J. Chemi. Ecol. 16:261–272.Google Scholar
  43. Rose, C. D., Sharp, W. C., Kenworthy, W. J., Hunt, J. H., Lyons, W. G., Prager, E. J., Valentine, J. F., Hall, M. O., Whitfield, P. E., and Fourqueran, J. W. 1999. Overgrazing of a large seagrass bed by the sea urchin Lytechinus variegatus in outer Florida Bay. Mar. Ecol. Prog. Seri. 190:211–222.Google Scholar
  44. Skajaa, K., Ferno, S., and Lokkeborg, H. E. K. 1998. Basic movement pattern and chemo-oriented search towards baited pots in edible crab (Cancer pagurus L.). Hydrobiologia 371/372:143–153.Google Scholar
  45. Sorensen, P. W. and Caprio, J. 1997. Chemoreception, pp. 375–405 in D. H. Evans, (ed.). The Physiology of Fishes. CRC Press, Boca Raton, Florida.Google Scholar
  46. Steullet, P. and Derby, C. D. 1997. Coding of blend ratios of binary mixtures by olfactory neurons in the Florida spiny lobsterm Paulirus argus. J. Comp. Physiol. 180: 123–135.Google Scholar
  47. Strong, D. L. 1992. Are trophic cascades all wet? Differentiation and donor control in speciose ecosystems. Ecology 73:747–754.Google Scholar
  48. Tamburri, M. N. and Barry, J. P. 1999. Adaptations for scavenging by three diverse bathyl species, Eptatretus stouti, Neptunea amianta and Orchomene obtusus. Deep-Sea Res. 46:2079–2093.Google Scholar
  49. Tertschnig, W. P. 1989. Diel activity patterns and foraging dynamics of the sea urchin Tripneustes ventricosus in a tropical seagrass community and a reef environment (Virgin Islands). P.S.Z.N. I: Mar. Ecol. 10:3–21.Google Scholar
  50. Trussel, G. C. 1996. Phenotypic plasticity in an intertidal snail: the role of a common predator. Evolution 40:448–454.Google Scholar
  51. Vickers, N. J. 2000. Mechanisms of animal navigation in odor plumes. Biol. Bull. 198:203–212.Google Scholar
  52. Virnstein, R.W. 1977. The importance of predation by crabs and fishes on benthic infauna in Chesapeake Bay. Ecology 58:1199–1217.Google Scholar
  53. Voigt, R. L. and Atema, J. 1992. Tuning of chemoreceptor cells of the second antennae 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
  54. Webster, D. R. and Weissburg, M. J. 2001. Chemosensory guidance cues in a turbulent odor plume. Limnol. Oceanogr. 46:1048–1053.Google Scholar
  55. Webster, D. R., Rahman, S., and Dasi, L. P. (2002) Laser-induced fluorescence measurements of a turbulent plume. ASCE J. Eng. In press.Google Scholar
  56. Weissburg, M. J. 2000. The fluid dynamical context of chemosensory behavior. Biol. Bull. 198:188–202.Google Scholar
  57. Weissburg, M. J. and Derby, C. D. 1995. Regulation of sex-specific feeding behavior in fiddler crabs: Physiological properties of chemoreceptor neurons in claws and legs of males and females. J. Comp. Physiol. A. 176:513–526.Google Scholar
  58. Weissburg, M. J. and Zimmer-Faust, R. K. 1993. Life and death in moving fluids: Hydrodynamic effects on chemosensory-mediated predation. Ecology 74:1428–1443.Google Scholar
  59. Weissburg, M. J. and Zimmer-Faust, R. K. 1994. Odor plumes and how blue crabs use them to find prey. J. Expet. Biol. 197:349–375.Google Scholar
  60. Weissburg, M. J., Dusenbery, D. B. Ishida, H., Janata, J., Keller, T., Roberts, P. J. W., and Webster, D. R. 2002. A multidisciplinary study of spatial and temporal scales containing information in turbulent chemical plume tracking. J. Environ. Fluid Mech. 2:65–94. 1970 WEISSBURG, FERNER, PISUT, AND SMEEGoogle Scholar
  61. Wight, K., Francis, L., and Eldridge, D. 1990. Food aversion learning by the hermit crab Pagurus granosimanus. Biol. Bull. 178:205–209.Google Scholar
  62. Woodin, S. A. 1983. Biotic interactions in recent marine sedimentary environments. pp. 3–38 in M. J. S. Tevesz and P. L. McCall (eds.). Biotic Interactions In Recent and Fossil Benthic Communities. Plenum Press, New York.Google Scholar
  63. Wright, L. D. 1989. Benthic boundary layers of estuarine and coastal environments. Rev. Aquat. Sci. 1:75–95.Google Scholar
  64. Wright, S. H. and Manahan, D. T. 1989. Integumental nutrient uptake by aquatic organisms. Annu. Rev. Physiol. 51:585–600.Google Scholar
  65. Zimmer, R. K., Commins, J. E., and Browne, K. A. 1999. Regulatory effects of environmental chemical signals on search behavior and foraging success. Ecology 80:1432–1446.Google Scholar
  66. Zimmer-Faust, R. K. 1989. The relationship between chemoreception and foraging behavior in crustaceans. Limnol. Oceanogr. 34:1367–1374.Google Scholar
  67. Zimmer-Faust, R. K. 1993. ATP: a potent prey attractant evoking carnivory. Limnol. Oceanogr. 38:1271–1275.Google Scholar
  68. Zimmer-Faust, R. K. and Butman, C. A. 2000. Chemical signaling processes in the marine environment. Biol. Bull. 198:168–187.Google Scholar
  69. Zimmer-Faust, R. K. and Case, J. F. 1982a. Odors influencing foraging behavior of the California spiny lobster,Panulirus interruptus, and other decapod Crustaceans. Mar. Behav. Physiol. 9:35–38.Google Scholar
  70. Zimmer-Faust, R. K. and Case, J. F. 1982b. Organization of food search in the kelp crab Pugettia producta (Randall). J. Expe. Mar. Biol. Ecol. 57:237–255.Google Scholar
  71. Zimmer-Faust, R. K., Stanfill, J. M., and Collard, S. B. III. 1988. Afast multi-channel fluorometer for investigating aquatic chemoreception and odor trails. Limnol. Oceanogr. 33:1586–1595.Google Scholar
  72. Zimmer-Faust, R. K., Finelli, C. M., Pentcheff, N. D., and Wethey, D. S. 1995. Odor plumes and animal navigation in turbulent water flow. A field study. Biol. Bull. 188:111–116.Google Scholar

Copyright information

© Plenum Publishing Corporation 2002

Authors and Affiliations

  • Marc J. Weissburg
    • 1
  • Matthew C. Ferner
    • 1
  • Daniel P. Pisut
    • 1
  • Delbert L. Smee
    • 1
  1. 1.School of BiologyGeorgia Institute of TechnologyAtlantaUSA

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