In a recent experiment designed to figure out how the microbiome of tadpoles was influenced by other animal species in the environment, my colleagues and I studied healthy communities of freshwater bacteria, crustaceans and insects from wetland habitats in the Brazilian Atlantic Forest. We focused on their feeding activities — how they filtered water to get their food and broke down dead plant material.

It is well known that these feeding activities are essential for ecosystem functions such as decomposition. But we found that these food webs also served another purpose: They boosted growth of "good" bacterial species in the environment, such as species that fight pathogenic microbes.

As a result, tadpoles sharing the ecosystem with these microorganisms and invertebrates had healthier gut microbiomes. This provided a strong defense against pathogens, compared with tadpoles that weren’t sharing their habitat with diverse networks of organisms.

Mapping species interactions in diverse ecosystems is difficult under field conditions, where the environment is unpredictable, and replicating experiments to confirm findings is challenging.

Tightly whorled leaves of bromeliad plants provide a mini-aquarium for tadpoles, invertebrates and microorganisms. Photo by Sasha Greenspan
Bromeliads are ideal for experimental work on community interactions because they are natural microcosms and their small dimensions allow for us to grow many of them in a small space. Our study sites in Brazil’s tropical rainforests support extremely high densities of bromeliads from ground to canopy, often resembling a Dr. Seussian wonderland.

To recreate natural ecosystems for our experiment, we planted a garden of 60 identical bromeliads outdoors in the shade of a small tropical forest in São Paulo, Brazil. We then allowed the bromeliads to be naturally colonized by invertebrates and microorganisms for three months. Some plants were exposed to ambient temperatures, and others were warmed up to 6 degrees above ambient — with a custom outdoor heating system — to match predicted global climate change trends.

Nearby, we collected our model host species for the experiment — tadpoles of the treefrog species Ololygon perpusilla that breed only in the mini-aquariums created by the leaves of bromeliads.

We then transferred the bromeliads from outdoors into the lab, added a tadpole to the tiny pool of water at the center of each plant and applied the same heating system to simulate warming. After a few weeks, we inventoried the bacterial species in the tadpole intestines as well as the bacteria and invertebrate species living in the bromeliads.

The domino effects of climate change

The health of tadpole gut microbiomes specifically was linked to changes in the community of aquatic bacteria and invertebrates living alongside tadpoles within the bromeliads. That is, warming supported growth and reproduction of certain species of bacteria and invertebrates and inhibited others, and these environmental changes disturbed the tadpole gut microbiome.

The higher temperatures also led to faster development of filter-feeding mosquito larvae. Our results suggest that higher rates of filter-feeding also altered the species composition of bacteria in the environment in ways that further disturbed the tadpole microbiome.

In fact, tadpole growth — a proxy for the species’ health — was more strongly associated with warming-induced shifts in their gut microbiomes than with direct effects of warming on growth that are expected in cold-blooded animals such as tadpoles or effects of warming on the tadpoles’ algal food resources.

Our work demonstrates how global-scale climate change can affect even the smallest levels of biological organization, including the symbiotic bacteria living within the digestive tract of a tiny frog species.

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Microbiology :Current Research