CRAYFISH FEEDING PREFERENCES FOR FRESHWATER MACROPHYTES: THE INFLUENCE OF PLANT STRUCTURE AND CHEMISTRY

Abstract The omnivorous crayfish Procambarus clarkii fed selectively on several species of macrophytes, preferring delicate fresh plants that had filamentous or finely-branched architectures. When the macrophytes were dried, powdered, and reconstituted into an alginate gel (thus eliminating among-species differences in physical characteristics), crayfish preferences were altered; previously tough plants that were high in nitrogen and protein were preferred over previously delicate plants that were low in nitrogen and protein. Even though plant structure influences feeding decision of crayfish, the structurally identical macrophyte gels were fed upon differently, demonstrating that nonstructural traits are important feeding determinants. However, plant tissue constituents such as nitrogen, protein, phenolics, lignin, cellulose, or ash were not significantly correlated with feeding preferences. Two high-nitrogen plants that were avoided by crayfish as fresh and as reconstituted tissue (Nuphar luteum macrophyllum and Alternanthera philoxeroides) possessed extracts that reduced crayfish feeding in laboratory assays, demonstrating that macrophyte metabolites can deter some herbivores. As is often observed with large generalist herbivores and omnivores in terrestrial and marine systems, the freshwater crayfish made feeding decisions based upon multiple plant cues (structure, nutrition, chemical defenses).

[1]  G. Cronin Influence of Macrophyte Structure, Nutritive Value, and Chemistry on the Feeding Choices of a Generalist Crayfish , 1998 .

[2]  Stephen R. Carpenter,et al.  Effects of submersed macrophytes on ecosystem processes , 1986 .

[3]  B. Baker,et al.  Marine Chemical Ecology , 2001 .

[4]  R. Newman,et al.  The watercress glucosinolate-myrosinase system: a feeding deterrent to caddisflies, snails and amphipods , 1992, Oecologia.

[5]  E. Zettler,et al.  Chemical Defences in Aquatic Plants , 1986 .

[6]  J. Emmett Duffy,et al.  Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes , 1992, Oecologia.

[7]  V. Paul,et al.  Activation of chemical defenses in the tropical green algae Halimeda spp. , 1992 .

[8]  M. Berenbaum,et al.  Herbivores: their interactions with secondary plant metabolites, vol. II: ecological and evolutionary processes. , 1992 .

[9]  D. Lodge,et al.  Comparative feeding selectivity of herbivorous insects on water lilies: aquatic vs. semi‐terrestrial insects and submersed vs. floating leaves , 1998 .

[10]  A. Covich,et al.  Effects of an omnivorous crayfish (Orconectes rusticus) on a freshwater littoral food web , 1994 .

[11]  D. Janzen,et al.  Herbivores: Their Interaction With Secondary Plant Metabolites , 1982 .

[12]  E. Chavez,et al.  Aquatic feeding by moose: selection of plant species and feeding areas in relation to plant chemical composition and characteristics of lakes , 1984 .

[13]  D. Lodge,et al.  Multi-Trophic-Level Impact of Sublethal Interactions between Bass and Omnivorous Crayfish , 1995, Journal of the North American Benthological Society.

[14]  D. Lodge,et al.  Reductions in Submersed Macrophyte Biomass and Species Richness by the Crayfish Orconectes rusticus , 1987 .

[15]  E. O. Beal A manual of marsh and aquatic vascular plants of North Carolina with habitat data , 1977 .

[16]  C. Montes,et al.  DIET OF THE RED SWAMP CRAYFISH PROCAMBARUS CLARKII IN NATURAL ECOSYSTEMS OF THE DONANA NATIONAL PARK TEMPORARY , 1998 .

[17]  K. Cummins,et al.  An Introduction to the Aquatic Insects of North America , 1981 .

[18]  W. J. Conover,et al.  Practical Nonparametric Statistics , 1972 .

[19]  P. Steinberg,et al.  Chapter 10 – The Chemical Ecology of Plant–Herbivore Interactions in Marine versus Terrestrial Communities , 1992 .

[20]  M. Ragan,et al.  Phenolic compounds in brown and red algae , 1978 .

[21]  W R Rice,et al.  'Heads I win, tails you lose': testing directional alternative hypotheses in ecological and evolutionary research. , 1994, Trends in ecology & evolution.

[22]  J. Burke,et al.  The impact of the crayfish Orconectes virilis on aquatic macrophytes , 1990 .

[23]  Michael S. Deal,et al.  Bioassays with Marine and Freshwater Macroorganisms , 1998 .

[24]  D. Lodge,et al.  Feeding preferences and performance of an aquatic lepidopteran on macrophytes: plant hosts as food and habitat , 2001, Oecologia.

[25]  F. Provenza Postingestive Feedback as an Elementary Determinant of Food Preference and Intake in Ruminants , 1995 .

[26]  D. Lodge,et al.  Impact of Herbivory on Plant Standing Crop: Comparisons Among Biomes, Between Vascular and Nonvascular Plants, and Among Freshwater Herbivore Taxa , 1998 .

[27]  W. Momot Redefining the role of crayfish in aquatic ecosystems , 1995 .

[28]  W. J. Mattson,et al.  Herbivory in relation to plant nitrogen content , 1980 .

[29]  H. Damman Leaf Quality and Enemy Avoidance by the Larvae of a Pyralid Moth , 1987 .

[30]  N. Lindquist,et al.  Chemical Defenses of Freshwater Macrophytes Against Crayfish Herbivory , 2004, Journal of Chemical Ecology.

[31]  E. B. Coleman,et al.  Red swamp crawfish: biology and exploitation , 1984 .

[32]  R. Newman Herbivory and Detritivory on Freshwater Macrophytes by Invertebrates: A Review , 1991, Journal of the North American Benthological Society.

[33]  S. Watts,et al.  Behavioral (Feeding) Responses of the Crayfish, Procambarus clarkii, to Natural Dietary Items and Common Components of Formulated Crustacean Feeds , 2004, Journal of Chemical Ecology.

[34]  G. Cronin,et al.  Within-plant variation in seaweed palatability and chemical defenses: optimal defense theory versus the growth-differentiation balance hypothesis , 1996, Oecologia.

[35]  E. Prepas,et al.  The effect of aquatic plant chemistry and morphology on feeding selectivity by the crayfish, Orconectes virilis , 1991 .

[36]  W. Fenical,et al.  Synergisms in Plant Defenses against Herbivores: Interactions of Chemistry, Calcification, and Plant Quality , 1994 .

[37]  C. Montes,et al.  Diet of the Red Swamp Crayfish Procambarus Clarkii in Natural Ecosystems of the Doñana National Park Temporary Fresh-water Marsh (Spain) , 1998 .

[38]  C. Peterson,et al.  Analysis of feeding preference experiments , 1989, Oecologia.

[39]  G. Cronin,et al.  Susceptibility to Herbivores Depends on Recent History of both the Plant and Animal , 1996 .

[40]  J. Emmett Duffy,et al.  Herbivore Resistance to Seaweed Chemical Defense: The Roles of Mobility and Predation Risk , 1994 .

[41]  M. Littler,et al.  The Evolution of Thallus Form and Survival Strategies in Benthic Marine Macroalgae: Field and Laboratory Tests of a Functional Form Model , 1980, The American Naturalist.

[42]  D. Lodge Herbivory on freshwater macrophytes , 1991 .

[43]  G. Cronin,et al.  Effects of storage and extraction procedures on yields of lipophilic metabolites from the brown seaweeds Dictyota ciliolata and D. menstrualis , 1995 .

[44]  I. Valiela,et al.  The role of phenolic compounds and other plant constituents in feeding by Canada geese in a coastal marsh , 1984, Oecologia.

[45]  J. Fryxell,et al.  The Effect of Nutritional Quality on Forage Preference by Beavers , 1993 .

[46]  Richard Karban,et al.  Induced Responses to Herbivory , 1997 .

[47]  M. M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. , 1976, Analytical biochemistry.

[48]  G. Cronin,et al.  Are Tropical Herbivores More Resistant Than Temperate Herbivores to Seaweed Chemical Defenses? Diterpenoid Metobolites from Dictyota acutiloba as Feeding Deterrents for Tropical Versus Temperate Fishes and Urchins , 1997, Journal of Chemical Ecology.

[49]  R. Creed Direct and indirect effects of crayfish grazing in a stream community , 1994 .