Can Quantity Replace Quality? Food Choice, Compensatory Feeding, And Fitness Of Marine Mesograzers

Ecology, Jan, 2000 by Edwin Cruz-Rivera, Mark E. Hay

EDWIN CRUZ-RIVERA [1,3]

MARK E. HAY [2,4]

Abstract. Relationships among food choice, compensatory feeding, and the consequences for consumer fitness rarely have been quantified. We created foods of varying nutritional quality and evaluated the consequences of compensatory feeding for three sympatric species of amphipods by analyzing food choices, feeding rates, and long-term effects on fitness. Nutritional quality was manipulated by creating low-quality diets from algae (low in protein, nitrogen, and total organic carbon), high-quality diets from commercial fish food (high in protein, nitrogen, and total organic carbon), and intermediate-quality diets from mixtures of those two foods. When high- and low-quality diets were simultaneously offered, the more mobile, non-tube-building amphipods, Gammarus mucronatus and Elasmopus levis, both fed preferentially on the high-quality diet. The more sedentary, tube-building amphipod Ampithoe longimana did not discriminate between these foods. When confined to a single food type, all three species exhibited com pensatory feeding on the low-quality diet. Despite compensatory feeding, when Elasmopus levis were cultured on the low-quality food, they experienced reduced survivorship, growth, and fecundity during two successive ovulations, compared to individuals feeding on more nutrient-rich foods. Low-nutrient foods caused similar declines in growth and female gonad size for Gammarus mucronatus. In contrast, the survivorship, growth, and fecundity of Ampithoe longimana was not affected by any of the diets tested. Thus, compensatory feeding allowed the more sedentary species, Ampithoe longimana, to completely circumvent the effects of low nutritional quality, but the same behavior was ineffective for both of the more mobile species, Gammarus mucronatus and Elasmopus levis. The ability of A. longimana to achieve equal fitness by substituting food quantity for food quality may allow this sedentary species to form longer associations with individual host plants, minimize movement among hosts, and thus lower its risk of bei ng detected by predators.

Key words. amphipods; Ampithoe longimana; compensatory feeding; diet and fitness; Elasmopus levis; food choice and fitness of marine amphipods; Gammarus mucronatus; marine mesograzers; relative mobility and predation risk; nutrition.

INTRODUCTION

Investigations of how chemical, structural, morphological, or nutritional traits affect prey susceptibility to consumers are common (Hay and Fenical 1988, 1996, Duffy and Hay 1990, Harvell 1990, Fritz and Simms 1992, Hay and Steinberg 1992, Paul 1992, Rosenthal and Berenbaum 1992, Pawlik 1993, Hay 1996). It is rare, however, to demonstrate that these same traits actually affect consumer fitness, especially in marine systems (Hay 1996; but see Lindquist and Hay [1995]). Thus, for many marine consumers, the direct effects of prey traits on consumer fitness are poorly documented. Although low nutritional value often has been hypothesized to deter consumers (Feeney 1976, Moran and Hamilton 1980, Price et al. 1980, White 1993, Augner 1995), this hypothesis is controversial because consumers may compensate for low prey quality by consuming more, rather than less, prey tissue (Price et al. 1980).

Studies on the physiology and ecology of nutrition in humans, ruminants, insects, and other terrestrial animals have documented the impact of food quality on the feeding behavior and performance of consumers (Slansky and Scriber 1985, Slansky and Rodriguez 1987, Widdowson and Mathers 1992, Slansky 1993, Van Soest 1994), and have facilitated development of broadly applied theories, such as optimal foraging and optimal diet selection. In general, higher quality foods enhance fitness and should be selectively eaten when available (reviewed by Stephens and Krebs [1986]). Alternatively, some consumers actively mix different foods to achieve a more balanced diet, or to dilute detrimental chemicals that would accumulate to harmful concentrations if consumers fed extensively on one species of prey (Pennings et al. 1993, Bernays et al. 1994).

Consumers, however, may not always have access to high-quality or complementary foods, because natural enemies, competitors, or abiotic stresses limit consumer distribution and behavior (Sih 1987, Real and Caraco 1986, Huang and Sih 1991, Posey and Hines 1991, Stachowicz and Hay 1999b). When environmental constraints confine consumers to lower quality diets, consumers may still obtain sufficient nutrients, if they can compensate by increasing their consumption rate or assimilation efficiency (Simpson and Simpson 1990). Although compensation on lower quality foods has been observed for numerous consumers (Simpson and Simpson 1990, Rueda et al. 1991, Targett and Targett 1990, Graca et al. 1993, Pennings et al. 1993, Stachowicz and Hay 1996), few studies have evaluated how well compensatory feeding offsets the effects of low food quality on consumer fitness.

Several terrestrial studies of compensatory feeding have focused on small herbivores, such as insects and slugs (e.g., Slansky and Scriber 1985, Simpson and Simpson 1990, Rueda et al. 1991, Slansky 1993). Similar investigations of small marine herbivores (e.g., mesograzers such as amphipods, polychaetes, isopods, or small crabs, shrimps, and gastropods) are generally lacking. Because enemies or physical rigors limit the time or space over which mesograzers can forage (Lubchenco and Gaines 1981, Bernays and Graham 1988, Duffy and Hay 1991b, 1994), compensatory feeding might benefit mesograzers both directly (food acquisition) and indirectly (by reducing movement among hosts and thus lowering susceptibility to predation; Stachowicz and Hay 1996, 1999b).