Life and Death in Moving Fluids: Hydrodynamic Effects on Chemosensory‐Mediated Predation

Previous studies in taxonomically diverse marine animals have established the general existence, and importance, of the olfactory sense in a wide variety of behavioral processes. Evidence suggests that the sense of smell mediates predatory search in many marine animals. Past investigations have not, however, been designed to link either the degree of successful olfactory-mediated search or guidance mechanisms with the hydraulic environment in which predatory activities naturally take place. In an effort to examine the interaction between hydrodynamics and chemoreception, we investigated predatory success and search strategies of blue crabs foraging in controlled hydrodynamic environments generated in a flume. Hydrodynamics were characterized by quantifying boundary layer shear velocity (u*) and roughness Reynolds number (Re.), two measures that describe the structure of boundary layer flows. Flow properties affected the ability of crabs to orient to odor plumes emanating from actively pumping infaunal bivalves (Mercenaria mercenaria). High flow speed or large sediment particle size increased boundary layer turbulence, thereby decreasing the success of crab chemo-orientation ability. In addition, high flow speed also lessened the probability that crabs contacted odor plumes. Thus, habitats with high flows can provide hydrodynamic refuges from olfactory-mediated predation. Because search ability is contingent on the magnitude of boundary layer turbulence, olfactory-mediated predation may also be ineffective in slow flows, if bottom roughness elements can generate sufficient turbulence. Further, search ability in blue crabs is extremely sensitive to small changes in benthic boundary layer structure. The presence of a thick viscous sublayer, dominated by quasilaminar flow, seems especially critical for successful location of an odor source by crabs. Benthic estuarine crustaceans inhabit an environment where flows are transitional between smooth- and rough-turbulent conditions. Accordingly, chemosensory systems appear geared primarily to extracting information from hydraulically smooth flows. These results indicate that mechanisms governing the physical transport of odor signals can have profound influences, not only on the development of sensory and behavioral mechanisms, but also on biotic interactions such as predation, which, in turn, can mediate community structure.

[1]  L. Coen,et al.  The effect of long-term alteration of in situ currents on the growth of Mercenaria mercenaria in the northern Gulf of Mexico , 1992 .

[2]  E. J. List Turbulent Jets and Plumes , 1982 .

[3]  A. R. Nowell,et al.  FLUMES : THEORETICAL AND EXPERIMENTAL CONSIDERATIONS FOR SIMULATION OF BENTHIC ENVIRONMENTS* , 1987 .

[4]  H. Oliver Wind profiles in and above a forest canopy , 1971 .

[5]  S. Palumbi How body plans limit acclimation: responses of a demosponge to wave force , 1986 .

[6]  A. Sih Antipredator Responses and the Perception of Danger by Mosquito Larvae , 1986 .

[7]  A. Baggaley,et al.  Rate of excretion of ammonia by the hard clam Mercenaria mercenaria and the American oyster Crassostrea virginica , 1976 .

[8]  D. Wethey Ranking of settlement cues by barnacle larvae: influence of surface contour , 1986 .

[9]  M. Hadfield,et al.  Evidence for a soluble metamorphic inducer in Phestilla: ecological, chemical and biological data , 1985 .

[10]  T. L. Payne,et al.  Mechanisms in Insect Olfaction , 1986 .

[11]  A. Sih,et al.  Predator-prey interactions among fish and larval amphibians: use of chemical cues to detect predatory fish , 1987, Animal Behaviour.

[12]  R. Shaw,et al.  Structure of the Reynolds Stress in a Canopy Layer , 1983 .

[13]  E. Buskey Swimming pattern as an indicator of the roles of copepod sensory systems in the recognition of food , 1984 .

[14]  E. F. Bradley,et al.  Turbulent flow in a model plant canopy , 1976 .

[15]  P. Jumars,et al.  Effects of bivalve siphonal currents on the settlement of inert particles and larvae , 1988 .

[16]  C. Young,et al.  ORIENTATION AND CURRENT-INDUCED FLOW IN THE STALKED ASCIDIAN STYELA MONTEREYENSIS , 1980 .

[17]  D. Caldwell,et al.  Evidence for the influence of form drag on bottom boundary layer flow , 1982 .

[18]  E. R. Rumbo,et al.  Adaptation Processes in Insect Olfactory Receptors , 1987, Annals of the New York Academy of Sciences.

[19]  R. K. Zimmer-Faust The relationship between chemoreception and foraging behavior in crustaceans , 1989 .

[20]  M. Palmer,et al.  Dispersal of meiofauna in a turbulent tidal creek , 1985 .

[21]  P. Dunham SEX PHEROMONES IN CRUSTACEA , 1978 .

[22]  J. Spurrier,et al.  Carbon, nitrogen and phosphorus processing by an oyster reef , 1989 .

[23]  B. Ache,et al.  Olfaction: Responses of a Decapod Crustacean Are Enhanced by Flicking , 1979, Science.

[24]  Mark W. Denny,et al.  Nearshore Biomechanics. (Book Reviews: Biology and the Mechanics of the Wave-Swept Environment) , 1988 .

[25]  H. Fischer Mixing in Inland and Coastal Waters , 1979 .

[26]  R. Mathewson,et al.  CHEMOSENSORY ORIENTATION IN SHARKS * , 1971, Annals of the New York Academy of Sciences.

[27]  Steven Vogel,et al.  How much air passes through a silkmoth's antenna? , 1983 .

[28]  M. Weissburg,et al.  Ontogeny Versus Phylogeny in Determining Patterns of Chemoreception: Initial Studies with Fiddler Crabs. , 1991, The Biological bulletin.

[29]  R. Gleeson Pheromone communication in the reproductive behavior of the blue crab, Callinectes sapidus † , 1980 .

[30]  P. Morin,et al.  Effect of tidal currents, seston, and bottom sediments on growth of Mercenaria mercenaria: results of a field experiment , 1989 .

[31]  A. R. Nowell,et al.  Effects of Biological Activity on the Entrainment of Marine Sediments , 1981 .

[32]  Janet K. Thompson,et al.  A study of model bivalve siphonal currents , 1990 .

[33]  A fast, multichannel fluorometer for investigating aquatic chemoreception and odor trails , 1988 .

[34]  R. Soulsby,et al.  Measurements of the Reynolds stress components close to a marine sand bank , 1981 .

[35]  D. G. Hazen,et al.  Seabed Stresses in Combined Wave and Steady Flow Conditions on the Nova Scotia Continental Shelf: Field Measurements and Predictions , 1988 .

[36]  J. Himmelman Movement of whelks (Buccinum undatum) towards a baited trap , 1988 .

[37]  Ronald M. Cionco,et al.  A Mathematical Model for Air Flow in a Vegetative Canopy , 1965 .

[38]  L. Wright Benthic boundary layers of estuarine and coastal environments , 1989 .

[39]  C. A. Butman Larval Settlement of Soft-Sediment Invertebrates: Some Predictions Based on an Analysis of Near-Bottom Velocity Profiles , 1986 .

[40]  J. Atema,et al.  Spatial Information in the Three-Dimensional Fine Structure of an Aquatic Odor Plume. , 1991, The Biological bulletin.

[41]  M. Tamburri,et al.  Natural Sources and Properties of Chemical Inducers Mediating Settlement of Oyster Larvae: A Re-examination. , 1992, The Biological bulletin.

[42]  Peter B. Johnsen,et al.  Spatial gradient detection of chemical cues by catfish , 1980, Journal of comparative physiology.

[43]  R. Lipcius,et al.  Variable Functional Responses of a Marine Predator in Dissimilar Homogeneous Microhabitats , 1986 .

[44]  A. Holland,et al.  Influence of predation on infaunal abundance in Upper Chesapeake Bay, USA , 1980 .

[45]  T. Gross,et al.  Mean flow and turbulence scaling in a tidal boundary layer , 1983 .

[46]  P. Lawton,et al.  Portunid crab predation on juvenile hard clams: effects of substrate type and prey density , 1990 .

[47]  D. Rittschof,et al.  CHEMICAL ATTRACTION OF NEWLY HATCHED OYSTER DRILLS , 1983 .

[48]  B. L. Olla,et al.  CHEMORECEPTION IN THE BLUE CRAB, CALLINECTES SAPIDUS , 1977 .

[49]  A. Hines,et al.  Guild structure and foraging impact of blue crabs and epibenthic fish in a subestuary of Chesapeake Bay , 1990 .

[50]  L. Mullineaux,et al.  Initial contact, exploration and attachment of barnacle (Balanus amphitrite) cyprids settling in flow , 1991 .

[51]  B. Peckarsky Predator‐Prey Interactions between Stoneflies and Mayflies: Behavioral Observations , 1980 .

[52]  Pamela Reeder,et al.  Chemotaxis in the Florida spiny lobster, Panulirus argus , 1980, Animal Behaviour.