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Open Access Publications from the University of California

Microbes in time: Incorporating bacteria into ecosystem development theory

  • Author(s): Armitage, David
  • Advisor(s): Sousa, Wayne P
  • et al.

It is widely theorized that population and community processes such as competition, predation, and dispersal influence rates of resource flux within ecosystems. Likewise, the properties of an ecosystem, such as resource availability and space, can feed back onto populations and communities, driving their dynamics and evolutionary trajectories. However, empirical research connecting community and ecosystem-level processes remains a critical missing link between these two disciplines. My dissertation attempts to resolve some of these deficiencies by capitalizing on the tractability and replicability of experimental and natural microbial communities. I use these systems to test a number of theories of community-ecosystem feedbacks.

In chapter 1, I test the theory that a bioregion’s time-integrated area and productivity positively drive the extent of diversification in a radiating lineage. This theory of time-integration was developed in response to mismatches in the taxonomic diversity observed in a region (e.g., an island) compared to values predicted from species-area or species-productivity relationships. Time-integration implies that if a region’s historical area and productivity were higher than they are today, then its unexpectedly large biodiversity (for its contemporary area and/or productivity) might be explained by historical conditions favoring radiation and a persistence of many or all of these clades as area and/or productivity decreased. To test this theory, I used the bacterium Pseudomonas fluorescens SBW25 — a model system for adaptive radiation. I set up independent replicate microcosms that were randomly assigned to different volumes and productivities and transferred every few days so as to experience different environmental histories. By tracking these diversifying communities over time, I demonstrate that time-integrated productivity was the single best predictor of a community’s extant diversity whereas “snapshot” measures of contemporary volume and productivity are much less useful predictors. I interpret these results in the context of population growth parameters and extinction rates.

In chapter 2, I present the results of a field study of natural microbial digestive communities occupying leaves of the carnivorous pitcher plant Darlingtonia californica. I combine microscopy, biochemical assays, and community sequencing with respirometry and stable isotope pulse-chase experiments to examine how microbial community succession influences rates of detrital turnover, respiration, and nitrogen cycling in developing micro-ecosystems. I demonstrate that microbial community development and turnover in D. californica proceeds in parallel over time with communities becoming more similar to one another. These communities have considerably predictable dynamics such that the bacterial communities from one population can be used to quite accurately predict the ages of pitcher leaves in a different population and year. Furthermore, and in accordance with general successional theory, bacterial communities tended to display unimodal patterns in species diversity over time. This trend appeared driven by differences in the predicted functional properties of bacterial communities. I also encountered unimodal trends in rates of decomposition by the digestive community and nitrogen uptake efficiency by the host leaf. Bacterial diversity and bacterial and midge larvae biomass were positively associated with rates of decomposition, which in turn were positively associated with the efficiency of nitrogen uptake by the host leaf. This study is among the first to demonstrate predictable successional patterns and biodiversity-ecosystem functioning relationships in natural microbial communities.

In chapter 3, I present the results of a laboratory experiment demonstrating a decrease in the strength of biodiversity-ecosystem function (BEF) relationships and competitive interactions during succession in Darlingtonia californica leaves. It is often assumed that as ecosystems develop, competition-colonization tradeoffs or niche differences favor the gradual establishment of a biota more successful at competing for resources, leading to increased rates of competitive exclusion and shifting BEF relationships. My approach involved collecting bacterial strains from a cohort of leaves every 11 days over a one-year period and assembling them into communities of varying richness levels such that each community contained either 1, 2, 5, or 10 taxa also isolated from leaves of the same age. By employing an experimental design that allowed for the estimation of individual species’ effects as well as their interactions, I show that the relationship between community richness and carbon mineralization rates are most positive during early succession (22-55 days) and gradually decrease over time. Furthermore, diffuse competition was greatest during these same time periods. Together, these results suggest that the effects of species additions or removals on ecosystem processes can vary across time.

Chapter 4 presents an experiment testing a long-held assumption regarding the natural history of Darlingtonia californica. Specifically, I test the centuries-old assumption that the unique forked ‘fishtail appendage’ found on leaves of D. californica play an important role in the plant’s capture of arthropod prey. In a series of field experiments, I manipulated the presence/absence of the appendage on developing pitcher leaves and compared their prey compositions and biomass. I found that the absence of the fishtail appendage does not significantly impact prey capture success at the level of the individual leaf or within an entire population of leaves. Therefore, contrary to widespread beliefs, the fishtail appendage does not appear to be a critical adaptation enabling carnivory in this species. Instead, I propose three alternative scenarios for the evolutionary maintenance of this structure: 1) as a vestigial structure, 2) as a photosynthetic structure and 3) as a structure serving a potentially mutualistic role with the local insect community.

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