Intraspecific variations in delta13C indicate ontogenetic diet changes in deposit-feeding polychaetes

Ecology, June, 1998 by Brian T. Hentschel

INTRODUCTION

Identification of the food resources assimilated by detritivores in general and deposit feeders in particular is a difficult problem for ecologists (Lopez et al. 1989). To improve analyses of food webs Cohen et al. (1993) urged that consumers be grouped by species, but such distinctions are currently impossible among species that have vague diets dominated by "amorphous detritus" (e.g., Benke and Jacobi 1994) or "the organic fraction of ingested sediment" (Lopez and Levinton 1987). Cohen et al. (1993) added that when metaphoetesis (an ontogenetic change in diet) occurs, descriptions of food webs should distinguish among the size classes or life-cycle stages of that species. In this study, I present evidence of ontogenetic changes in diet within the free-living benthic forms of four species of deposit-feeding worms.

Many organisms undergo ontogenetic changes in niche; the best-known examples are amphibians, holometabolous insects, and many fishes (Werner and Gilliam 1984, Bergman and Greenberg 1994, Persson and Eklov 1995, Olson 1996). Many deposit feeders (and other benthic invertebrates) also have complex life cycles, beginning as planktonic larvae before shifting to a benthic existence (Thorson 1950). Ontogenetic niche changes also can occur continuously during growth, without a discrete metamorphosis or change in habitat (Polis 1984).

Accumulating evidence suggests that benthic juveniles of deposit-feeding species might change diet as they grow. By definition, deposit feeders ingest nutritionally poor material that is diluted with completely nonnutritive mineral grains (Lopez and Levinton 1987). Larvae of deposit feeders, on the other hand, ingest relatively high-quality diets (plankton or yolk). After settlement, juveniles face a transition from the rich larval diet to a poor adult one, and a digestive constraint associated with small body size (Penry and Jumars 1990) might make an abrupt shift to deposit feeding difficult (Jumars et al. 1990). Because gut volume scales as body volume to a power of 1.0 (Penry and Jumars 1990), while gut throughput rate scales to a power of 0.77 (Cammen 1980), gut residence time (volume/throughput rate) - and the extent to which material can be digested in the gut - will increase with body size (Penry and Jumars 1990). This size-dependent digestive constraint could be eased by either (1) an ontogenetic decrease in gut residence time or (2) ingestion of a higher quality diet during juvenile stages. Forbes (1989) measured a break in the allometry of throughput rate ([approximately equal to] egestion rate) for juveniles of Capitella sp. I, but the data show a shift from an allometric exponent of 1.21 to 0.78 at a body volume of 1.7 [mm.sup.3]. This implies, and direct measurements of gut residence time confirm, that the gut residence times of juveniles will be even shorter than would be predicted from the adult's allometric exponent (Forbes 1989). Given this scaling, ingesting a diet that can be digested more quickly than that of conspecific adults is the most likely means for juveniles to overcome the size-dependent digestive constraint (Jumars et al. 1990, Penry and Jumars 1990). Similar arguments that smaller individuals require diets that can be more easily digested have been made and confirmed for many other animals that ingest low-quality forage (Sibly 1981, Demment and Van Soest 1985, Caceres et al. 1994, Moir 1994).

One potential means for deposit-feeding juveniles to increase diet quality is to selectively ingest smaller particles that will increase the amount of surface-associated organic matter per unit volume of ingested sediment (Taghon et al. 1978). Intuition and interspecific relationships between body size and particle-size selection suggest a positive relationship between body size and the size of ingested particles, but at least some deposit-feeding worms show the opposite trend: smaller juveniles have a bias toward contacting and ingesting relatively larger particles more frequently than do conspecific adults (Hentschel 1996). Given the negative relationship between particle size and the quantity of surface-associated organic matter per unit volume (DeFlaun and Mayer 1983), this ontogenetic change in particle selection imposes an additional constraint on juveniles - not a means to overcome the digestive constraint associated with small gut size.

Scaling of gut size and feeding structures probably forces benthic juveniles to forage differently from the microphagous deposit- or suspension-feeding adults (Jumars et al. 1990). Because the morphology of juvenile and adult feeding structures can be quite similar (often only a change in the size of feeding structures occurs), any ontogenetic changes in foraging behaviors are probably subtle and likely involve gradations between general feeding guilds (e.g., Fauchald and Jumars 1979). Hentschel (1996), for example, speculates that an ontogenetic shift in the foraging behaviors of spionid polychaetes would increase diet quality if (1) juveniles spend more time than adults suspension feeding rather than deposit feeding (supported by unpublished data from G. Taghon) or (2) juveniles forage in a more macrophagous mode where only the higher quality organic components are ingested (i.e., a feeding mode that is more similar to that of many permanent meiofauna than to that of deposit-feeding macrofauna).