Strong interactions between stoichiometric constraints and algal defenses: evidence from population dynamics of Daphnia and algae in phosphorus-limited microcosms.

The dynamic interactions among nutrients, algae and grazers were tested in a 2 × 3 factorial microcosm experiment that manipulated grazers (Daphnia present or absent) and algal composition (single species cultures and mixtures of an undefended and a digestion-resistant green alga). The experiment was run for 25 days in 10-L carboys under mesotrophic conditions that quickly led to strong phosphorus limitation of algal growth (TP is approximately equal to 0.5 µM, N:P 40:1). Four-day Daphnia juvenile growth assays tested for Daphnia P-limitation and nutrient-dependent or grazer-induced algal defenses. The maximal algal growth rate of undefended Ankistrodesmus (mean ± SE for three replicate microcosms; 0.92 ± 0.02 day(-1)) was higher than for defended Oocystis (0.62 ± 0.03 day(-1)), but by day 6, algal growth was strongly P-limited in all six treatments (molar C:P ratio >900). The P-deficient algae were poor quality resources in all three algal treatments. However, Daphnia population growth, reproduction, and survival were much lower in the digestion-resistant treatment even though growth assays provided evidence for Daphnia P-limitation in only the undefended and mixed treatments. Growth assays provided little or no support for simple threshold element ratio (TER) models that fail to consider algae defenses that result in viable gut passage. Our results show that strong P-limitation of algal growth enhances the defenses of a digestion-resistant alga, favoring high abundance of well-defended algae and energy limitation of zooplankton growth.

Ontogeny of digestion in Daphnia: implications for the effectiveness of algal defenses.

Models of feeding and digestion predict that increased body size should result in longer gut passage time and improved assimilation efficiency. We examined the implications of digestion theory for size-structured interactions in a generalist zooplankton herbivore by studying the relationships between body size, ingestion rate, gut passage time (GPT), assimilation efficiency (AE), and growth rate in a clone of Daphnia pulex feeding on seven taxa of green algae that differed in digestibility. We also tested the effect of varying food concentration on GPT and AE while keeping body size constant. Food quality varied markedly among algal taxa, with mean juvenile growth rates at high food concentrations (1-2 mg/L) ranging from 0.10 to 0.61 d(-1). Juvenile growth rate for high food concentrations was highly correlated with juvenile AE (r2 = 0.96), verifying the importance of digestibility for food quality. AE, measured with 14C-labeled algae, increased with increasing age and body size for each of four digestion-resistant taxa but did not vary with age and body size for three readily digested algae. GPT decreased with decreasing body size, supporting the hypothesis that shorter GPT in juveniles leads to lower AE for digestion-resistant resources. Lower food concentrations led to increased GPT and improved AE for juveniles feeding on two digestion-resistant algae, providing further support for a role of longer gut retention in overcoming digestion defenses. The results suggest that increased abundance of digestion-resistant food will lead to growth and recruitment bottlenecks for juvenile herbivores, but that the effectiveness of digestion defenses will be decreased when large-bodied grazers predominate and when low food concentrations result in longer gut passage times. Gut processing constraints may favor either high concentrations of slow-growing, digestion-resistant resources or low concentrations of fast-growing, undefended resources.

Stoichiometry in an ecological context: testing for links between Daphnia P-content, growth rate and habitat preference.

We used laboratory experiments with ten Daphnia taxa to test for links between Daphnia P-content, growth rate and habitat preference. The taxa represent a wide range of body sizes and most show distinct preferences for one of three habitats: shallow lakes, deep, stratified lakes or fishless ponds. Previous studies show that taxa from shallow lakes and fishless ponds experience high predation risk and rich food resources, whereas taxa from deep lakes experience low predation risk, strong food limitation and potentially P-deficient resources. Thus, we predicted higher P-content and higher maximal growth rates in taxa from ponds and shallow lakes and lower P-content, lower maximal growth but reduced sensitivity to P-limitation in taxa preferring stratified lakes. In each of 25 experiments, a clonal Daphnia cohort was cultured for 4 days on a P-sufficient (molar C:P ratio 70) or a P-deficient (C:P 1,000) diet of a green alga at a high concentration (1 mg C l(-1)). The P-content of adult Daphnia fed the P-sufficient diet ranged from 1.52 to 1.22% mass. Small-bodied taxa from shallow lakes had higher P-content than larger-bodied taxa from deep lakes or fishless ponds. However, we found a nonsignificant negative correlation between P-content and growth on the P-sufficient diet, rather than the positive relationship predicted by the growth rate hypothesis. The P-deficient diet resulted in declines in both growth rate and P-content compared with the P-sufficient controls and the extent of the declines differed between taxa. Taxa from ponds showed a marginally greater decline in growth with the P-deficient diet compared with taxa from shallow or deep lakes. However, contrary to stoichiometric theory, no relationship was found between a species' P-content and growth depression on the P-deficient diet. Although we found evidence for habitat adaptations, our results show that factors other than Daphnia P-content are important in determining differences between Daphnia species in both maximal growth rate and sensitivity to P-limited growth.

Optimal foraging by a suspension-feeding copepod: responses to short-term and seasonal variation in food resources.

Laboratory radioisotope experiments were used to investigate the effects of phytoplankton seasonal succession on the selectivity and clearance rates of a suspension-feeding copepod in two Indiana lakes. Responses to particle size and quality were tested by allowing adult female Diaptomus birgei feeding in natural seston to select between a small (6×7 µm) flagellate (Chlamydomonas reinhardii) and a large, poor quality food (heat-killed Carteria olivieri, 22×25 µm). Short-term responses were tested in one lake by additional treatments in which copepods were acclimated for 5-6 h in filtered lake water ("starved") or natural seston with added Chlamydomonas ("enriched"). Copepods from both lakes fed selectively on the small live flagellate during the spring bloom of edible phytoplankton but fed selectively on the larger, poor quality particle during the "clear water phase" when food was scarce. These results are interpreted as an interaction between the concentration-dependent selectivity for high quality foods predicted by optimal diet theory and a perceptual bias for large-sized particles. Selectivity for high-quality food was intermediate and clearance rates were depressed when total phytoplankton abundance was high but dominated by filamentous cyanobacteria. In each experiment copepods also responded to the short-term manipulations by exhibiting weaker discrimination against the poor quality particle in the starvation treatment and stronger discrimination in the enriched treatment. A two-way mixed model ANOVA revealed substantial short term (37%) and seasonal (53%) components to the total variance in selectivity. Clearance rates were also influenced by both phytoplankton succession and the short-term resource manipulations. As expected, clearance rates on the poor quality food were more sensitive to the abundance of alternative foods. These results show how the feeding behavior of a freshwater copepod is modulated by both seasonal and short-term variation in natural food.

The role of taste in food selection by freshwater zooplankton.

Laboratory experiments with flavored and untreated polystyrene spheres revealed major differences in taste discrimination among diverse taxa of freshwater zooplankton. Copepods showed the strongest responses to flavor treatments. Both nauplii and copepodites of calanoid (Diaptomus) and cyclopoid (Cyclops) copepods selected flavored spheres over untreated ones. Moreover, a small cyclopoid, Tropocyclops, actively fed on an alga (Chlamydomonas) but did not ingest untreated spheres of the same size. Taste tests with cladocerans verified an overall tendency to ingest inert particles but also demonstrated important differences between families. Daphnids (4 species), Chydorus (Chydoridae) and Diaphanosoma (Sididae) did not respond to flavor treatments, while 2 species of bosminids selectively ingested flavored spheres. Daphnia also fed nonselectively in mixtures of algae and untreated spheres while Bosmina preferred algae over untreated spheres. Different species of rotifers exhibited 3 distinct responses to the flavor treatments: 1) Brachionus fed nonselectively, 2) Filinia fed preferentially on flavored 6 µm spheres, and 3) Polyarthra, Keratella, Synchaeta, and Noltholca infrequently ingested any spheres.Recent advances in our understanding of the feeding mechanisms of zooplankton help to explain why some taxa feed selectively on flavored particles while others do not. The ability of certain taxa to use taste to discriminate between high and low quality food particles has important implications for competition between zooplankton species and for interactions between planktonic grazers and their food resources.