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Ontogenetic and temporal shifts in the diet of the amphipod Gammarus fasciatus, in the Ohio River.

INTRODUCTION

Amphipods occupy a great diversity of lotic and lentic freshwater habitats, ranging in North America from the Laurentian Great Lakes to small headwater streams and large rivers such as the Mississippi (Bousfield, 1958); they are also common in troglobitic habitats (Thorp and Covich, 1991). In many aquatic ecosystems, amphipods in the common genus Gammarus comprise a significant portion of the benthic biomass throughout the year (Marchant, 1981). For example, G. fasciatus Say represented approximately 20% of the shallow-water biomass of the macrobenthos in the Ohio River near Louisville, Kentucky, before the invasion of the zebra mussel. Unlike some other lotic congeners (Gee, 1988), G. fasciatus does not appear to be food-limited (Delong et al., 1993); this may reflect food availability within its near-shore rock and macrophytic habitats, as well as an omnivorous diet.

Gammarid amphipods have been variously described as shredders, detritivores, scavengers, predators and omnivores (Clemens, 1950; Barlocher and Kendrick, 1973, 1975; Ladle, 1974; Moore, 1975; Willoughby and Sutcliffe, 1976; Marchant, 1981; Delong et al., 1993). The lack of food specificity may suggest variability in dietary preferences among species, differences in food availability among habitats and sampling season, or true omnivory. Even if most members of the genus Gammarus are omnivorous, this does not imply equal importance of the diverse food items for growth and development. Laboratory studies by Delong et al. (1993) showed that G. fasciatus was able to consume, assimilate and grow using three distinct food types: detritus (in the form of preconditioned leaves - both coarse particulate organic matter and fine particulate organic matter), filamentous algae (Cladophora spp.) and animal material (dead chironomids). Gammarus fasciatus grew fastest when feeding on animal material, followed in order by filamentous algae and detritus. As Delong et al. (1993) suggested, G. fasciatus may gain a certain advantage by concentrating on different food resources based on their seasonal or temporal abundances. A seasonal shift could account for the ability of G. fasciatus to grow and maintain significant year-round populations.

The goal of this study was to answer two key questions about the feeding ecology of Gammarus fasciatus in the Ohio River and in comparison to other amphipod species. First, do the composition and relative importance of food types in the diet of G. fasciatus shift seasonally in natural populations? Second, is there an ontogenetic shift in diet in natural populations? Answers to those questions will lead to greater understanding of amphipod feeding strategies, life history characteristics and their role in ecosystem processes.

MATERIALS AND METHODS

Analysis of diet. - Gammarus fasciatus were collected monthly for 1 yr (August 1991-July 1992; except in March when high-flow prevented sampling) in cobble beds of near-shore areas in the Ohio River near Louisville, Ky. Gammarus fasciatus were collected by washing medium-sized rocks with river water through a 200 [[micro]meter] sieve, fixed immediately in 10% formalin and later preserved in 70% ethanol. Head capsule lengths were measured in the laboratory using a dissecting microscope with an ocular micrometer and animals were placed in 0.1 mm size-class intervals. Size-class designations represented the maximum head length for amphipods in that group; for example, animals in the 0.5-mm size-class ranged from [greater than]0.4 to [less than or equal to]0.5 mm total head capsule length. Head capsule length has been shown to be effective for estimating total amphipod body size (Cooper, 1965; Martien and Benke, 1977). Delong et al. (1993) verified the correlation between head length and total length (total length = 8.778(head capsule length) - 1.0134; adjusted [R.sup.2] = 0.956; CV = 11.35).

Five G. fasciatus from each of the 0.5 to 1.6 mm size-classes from each monthly sample were dissected to examine gut contents. The foregut and midgut were removed and placed on a glass microscope slide. A drop of distilled water was added to distribute the gut contents evenly over the slide and the contents were examined using a compound light microscope. Forty evenly spaced fields were examined using a whipple disc at 100x and scored for the presence of filamentous algae, diatoms, animal matter and detritus. Filamentous algae and diatoms were identified by the presence of algal cells or frustules, either full or empty. Animal matter was identified by the presence of identifiable body parts or setae. Detritus was classified as all other unrecognizable material, including leaf matter and woody debris.

A weighted proportion method (Kesler et al., 1986; Delong et al., 1993) was used to determine the relative proportion of each food type in the diet. In this method, the number of fields scored positively for one food type was divided by the sum of all fields scored positively for all food types for an individual. This procedure was designed to compensate for differences in body size and gut fullness among individuals.

Statistical analyses. - Test of the data showed no significant departure from a normal distribution; therefore, parametric analyses were performed (SAS Institute Inc., 1990). The data were analyzed using MANOVA in a general linear model design. Differences among size classes and among months were tested for the three dependent variables (filamentous algae, diatoms and animal matter). Detritus was eliminated from the analysis since it occurred in every field for every size-class/month combination, and any differences in the relative proportion of detritus would be artifact of the changes in the other three food sources. Wilks' lambda and Pillai's trace F-approximations were used to test the hypotheses of overall size and month effects. Significance of all tests performed was [Alpha] = 0.05.

RESULTS

Dietary components. - Microscopic analysis of natural diet showed that the most common food type in the guts of Gammarus fasciatus was detritus, which occurred in each field scored (100%) for every individual analyzed. Filamentous algae (Chlorophyta and Cyanophyta) and diatoms (Bacillariophyta) were also major components of the diet, occurring at relative proportions of 0.036-0.287 and 0.061-0.281, respectively [ILLUSTRATION FOR FIGURE 1 OMITTED]. Animal matter comprised the least significant dietary component, with a relative proportion of 0.002-0.072 [ILLUSTRATION FOR FIGURE 1 OMITTED], and in all cases the relative proportion of animal matter was less than any of the other three food types. Animal matter found in the guts of G. fasciatus included the remains of oligochaetes, chironomids, zooplankton, freshwater sponges (spicules) and bryozoans (statoblasts).
TABLE 1. - General linear model multiple analysis of variance
(MANOVA) univariate results for each dependent variable. Factors are
significant if P [less than] 0.05

Source of variation         DF          MS        F          P

Variable: Filamentous Algae [R.sup.2] = 0.711 C.V. = 28.79

Model                       22       0.080      43.65      0.0001
Month                       10       0.010       5.67      0.0001
Size class                  12       0.108      58.74      0.0001
Month x size                68       0.001       0.09      0.0987
Error                      391       0.002

Variable: Diatoms [R.sup.2] = 0.566 C.V. = 41.70

Model                       22       0.067      23.15      0.0001
Month                       10       0.021       7.41      0.0001
Size class                  12       0.087      29.89      0.0001
Month x size                68       0.001       0.07      0.1276
Error                      391       0.003

Variable: Animal Matter [R.sup.2] = 0.433 C.V. = 59.58

Model                       22      0.0065      13.55      0.0001
Month                       10       0.002       3.94      0.0001
Size class                  12       0.007      15.19      0.0001
Month x size                89      0.0006       0.09      0.0785
Error                      391      0.0004


Effect of amphipod size on diet. - Relative proportions of filamentous algae, diatoms and animal matter rose with increasing amphipod size [ILLUSTRATION FOR FIGURE 1 OMITTED]. Results of MANOVA indicated significant differences within all food types with respect to amphipod size (Tables 1-2). The presence of filamentous algae increased linearly ([R.sup.2] = 0.711, P = 0.0001) from 0.036 at an amphipod head capsule length of 0.4 mm, to 0.287 at 1.6 mm head capsule length [ILLUSTRATION FOR FIGURE 1 OMITTED]. Similarly, diatoms rose from 0.061 to 0.281 ([R.sup.2] = 0.566, P = 0.0001) across the same head capsule length range (0.4-1.6 mm). Both filamentous algae and diatoms increased four-fold in relative proportion across the range of amphipod head capsule lengths. Animal matter increased three-fold across the same size range, ranging from 0.002 at 0.4 mm head capsule length to 0.072 at 1.6 mm head capsule length ([R.sup.2] = 0.433, P = 0.0001). No significant size-month interaction (P [greater than] 0.05) was present for any of the three dependent variables, indicating that amphipods of different sizes responded similarly with respect to month.
TABLE 2. - MANOVA test criterion and F approximations(1) for
hypotheses of no overall month or size class effect (using both
Wilks' Lambda and Pillai's Trace statistics)

Statistic                          Value       F           P

For overall month effect:

Wilks' Lambda                      0.667      5.64      0.0001
Pillai's Trace                     0.372      5.53      0.0001

For overall size class effect:

Wilks' Lambda                      0.219     21.45      0.0001
Pillai's Trace                     0.841     12.70      0.0001

1 H = Type III SS & CP matrices for month and size class E = error
SS & CP matrices


Monthly variation in weighted proportions. - MANOVA indicated a significant overall month effect on food type relative proportion (Tables 1-2) depending on month and specific food type. Filamentous algae, diatoms and animal matter increased in late winter through early-spring (January-April) [ILLUSTRATION FOR FIGURE 2 OMITTED]. Relative proportions of all food types were at their highest in April. In late spring (May), filamentous algae, diatoms and animal matter decreased substantially from their late winter early spring levels. Filamentous algae, diatoms and animal matter increased moderately in the summer (June-August), followed by a significant decrease for September. In late fall and early winter filamentous algae and animal matter increased, whereas diatoms increased through October and November, then significantly decreased in December.

DISCUSSION

Various aspects of feeding activity of the amphipod genus Gammarus have been widely studied, including functional feeding mode (Clemens, 1950; Barlocher and Kendrick, 1973; Ladle, 1974; Moore, 1975; Willoughby and Sutcliffe, 1976; Marchant, 1981; Marchant and Hynes, 1981; Dick, 1992; Friberg and Jacobsen, 1994), feeding rates (Marchant and Hynes, 1981), and the influence of food quality on growth (Gee, 1986; Delong et al., 1993; Pockl, 1995). While these studies offer considerable information about amphipod feeding ecology, most pertain to small streams and lakes and neglect amphipods in large rivers (Delong et al., 1993). Our results suggest that amphipods are important in large river ecosystems as omnivores that shift between food sources both temporally and ontogenetically.

Gammarus fasciatus has been previously described as an omnivore (Clemens, 1950; De-long et al., 1993); however, the types and relative proportions of food ingested seasonally have not been determined before this study. Our data indicate that G. fasciatus in the Ohio River consumed detritus (in the form of leaves, woody debris and other unrecognizable material), filamentous algae, diatoms and animal matter in varying proportions depending on amphipod size and month collected [ILLUSTRATION FOR FIGURE 1-2 OMITTED]. The difference in the abundances of the food types in the diet are reflected to some degree by their relative abundances in the Ohio River. Filamentous algae, detritus and diatoms are present year-round in significant amounts where G. fasciatus were collected. While animal matter is also available year-round, it is less abundant than the other forms of organic matter consumed by amphipods (R. B. Summers, pers. observ.).

Gammarus fasciatus changed foods with increasing size (and age). At small sizes, G. fasciatus was limited to a diet consisting of mainly detritus (regardless of month collected) with very little filamentous algae, diatoms and animal matter in their guts. As size increased, the proportions of filamentous algae, diatoms and animal matter in the diet increased nearly linearly up to the largest G. fasciatus. Large G. fasciatus consumed significant amounts of filamentous algae (0.25 relative proportion in diet), diatoms (0.22), and animal matter (0.07). The mechanism for this ontogenetic shift in food use is unclear, but one of two factors may be responsible. First, the shift may be related to a developmental phenomenon, whereby juvenile G. fasciatus are limited to a detrital diet because of the inability of their gnathopods or similar feeding mouthparts to handle larger food items (e.g., filamentous algae and invertebrate prey). A second explanation relates to size-specific competition among G. fasciatus, where large individuals exclude smaller conspecifics from the higher quality food items (filamentous algae, diatoms and living or dead animal matter). The first explanation has some experimental support by Delong et al. (1993) who demonstrated in a laboratory feeding experiment that small individuals of G. fasciatus showed a delayed growth response when fed algae (combination of filamentous and attached species) and animal matter. Growth was not delayed when juvenile G. fasciatus were fed only detritus (in the form of preconditioned, shredded leaves). A similar response was observed by Fuller and Stewart (1977) for the predaceous stonefly Isoperla fulva, where early instars were phytophagous until they grew to a sufficient size for predation. Some freshwater shredders (mainly Plecoptera and Trichoptera) become increasingly predaceous with increased body and mouthpart size (Lamberti and Moore, 1984). Increased diet breadth with increased size may lead to the advantages of higher growth rates and faster time to reproduction. Gammarus fasciatus appears to rely on a diet of primarily detritus until they are large enough to consume higher quality foods. The possibility of intraspecific competition cannot be eliminated, however, until tested experimentally.

Monthly analysis of gut contents showed a temporal shift in food use for natural populations of Gammarus fasciatus, irrespective of amphipod size. While there were no readily identifiable seasonal trends, there were significant monthly differences in all food types. The reasons for the significant monthly variations in all food types are unclear, largely due to our lack of quantitative information on the seasonal and monthly changes in food abundance within microhabitats in the Ohio River. For example, it is puzzling to note that filamentous algae, diatoms and animal matter were significantly reduced in G. fasciatus diets during April-May. We hypothesize that this is due to two factors: reproductive period and sedimentation rate. During the first reproductive period for G. fasciatus, males expend significant time and energy capturing, grasping and clinging to females. Also, this period followed an unusually high-flow flood event in March (recall we were unable to sample that month) which may have led to substantial sedimentation of the cobble beds as flood waters receded. These factors, alone or together, may explain the reduction in consumption of those food types.

Gammarus fasciatus is a significant component of the shallow-water macrobenthos in cobble and snag habitats in the Ohio River (Thorp, 1992). These cobble and snag habitats support a dense, year-round growth of filamentous algae and diatoms, as well as large numbers of small invertebrates. Gammarus fasciatus has shown the ability, in both laboratory studies (Delong et al., 1993) and our analysis of natural diet, to use these food resources year-round to varying degrees, depending on size and month collected. This ability to grow on a number of food sources reduces the chance that G. fasciatus will be food-limited at any size or time of year. Their omnivorous diet, along with their iteroparous life history strategy, may help account for the year-round success of Gammarus fasciatus in the Ohio River, as well as other habitats.

Acknowledgrnents. - The authors thank Kim Greenwood and David Kesler for comments and suggestions on gut content analysis and Gary Cobbs for statistical advice. The comments of two anonymous reviewers greatly improved the final manuscript.

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Author:Summers, R. Brent; Delong, M.D.; Thorp, J.H.
Publication:The American Midland Naturalist
Date:Apr 1, 1997
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