Integrating Bacteria into Food Webs: Studies with Sarracenia purpurea Inquilines

Abstract

Predation can have both direct and indirect effects on the population dynamics and community structure of freshwater plankton communities, but its effects on the bacterial component of aquatic systems are less well known. We used a series of laboratory reconstructions of the detritus-based food web in the leaves of the northern pitcher plant Sarracenia purpurea to test the hypothesis that interactions at higher trophic levels could control bacterial densities and community structure. The typical pitcher community is composed of a basal-level bacterial assemblage, bacterivorous protozoa and rotifers, and larvae of the pitcher plant mosquito Wyeomyia smithii.Using organisms isolated from natural pitchers, we constructed food webs comprising 1-4 consumer species (all possible combinations of the presence and absence of Colpoda, Cyclidium, Bodo, and Wyeomyia larvae) along with a constant bacterial species pool in a factorial design experiment. Bacterial community structure was modified by the direct effects of grazing by protozoa and mosquito larvae, by the indirect effects of competitive interactions among the three protozoans, and by the cascading effects of predation by mosquito larvae. Each combination of grazers/predators produced a different, species-specific pattern of bacterial species relative abundances. Changes in nutrient supplies and other abiotic characteristics of the microcosm environment resulting from the feeding activities of Wyeomyia and the protozoa also had indirect effects on bacterial species profiles. We found an apparent trophic cascade that was mediated by the species composition and relative abundances of the intermediate-level protozoan grazers.Our data support the hypothesis that Wyeomyia smithii serves as a keystone predator in the pitcher community. Mosquito larvae were responsible for the overall architecture of the pitcher food web and the subsequent interactions among grazers and the basal-level bacterial community. At low densities, mosquito larvae controlled patterns of coexistence among protozoan species by modifying competitive interactions, while at normal field densities, Wyeomyia rapidly drove the two ciliates to extinction but permitted continued existence of heterotrophic microflagellates. Wyeomyia larvae also played a dominant role in structuring the bacterial assemblage. Bacterial species profiles in food webs containing Wyeomyia were more similar to each other than to the patterns observed in webs without mosquito larvae.Our results suggest that the interactions among members of microbial communities are just as complex as those observed in plant and animal communities and require study at the species level. Because interactions among higher trophic levels can cascade down to the microbial level, it is therefore appropriate to consider the microbes as integral parts of the entire ecosystem, not merely as decomposers or food resources, but as fully interacting members of the community.

Diversity of Bacterial Communities in Container Habitats of Mosquitoes

“…Container habitats of mosquitoes are ecosystem mesocosms that are analogous to aquatic ecosystems that naturally occur in tree holes and other plant cavities [20]. These aquatic habitats support food webs that are dependent on detritus [8] and microbial communities that metabolize and mineralize organic carbon from detritus [29]. Based on sequence analysis of 16S rDNA amplicons, our investigation revealed that human-made water-filled containers and tree holes hold bacterial communities of mainly undescribed species.…”

Are natural microcosms useful model systems for ecology?

“…At the local (pitcher) scale, species diversity of many microscopic organisms (bacteria, rotifers and protozoa) is strongly affected by both TOP-DOWN (mosquito occurrence) and BOTTOM-UP (carcass provisioning) processes [7,9,13,22,46]. Mosquito occurrence at the pitcher scale is affected by bottom-up effects, such as carcass provisioning [43], carcass processing by midges [47] and pitcher size [43,48].…”

Predation, resource availability, and community structure in Neotropical water-filled tree holes

“…However, predators influence the diversity and abundance of some taxa (often other predators) living in the water held by pitcher plants (Addicott 1974;Cochran-Stafira and von Ende 1998), bromeliads (e.g., Lounibos et al 1987), Heliconia spp. bracts (Naeem 1988), bamboo stumps (Sota and Mogi 1996), and tree holes (e.g., Bradshaw and Holzapfel 1983;Fincke et al 1997;Nannini and Juliano 1998).…”