Abstract
In the Anthropocene, humans, domesticated animals, wildlife, and their environments are interconnected, especially as humans advance further into wildlife habitats. Wildlife gut microbiomes play a vital role in host health. Changes to wildlife gut microbiomes due to anthropogenic disturbances, such as habitat fragmentation, can disrupt natural gut microbiota homeostasis and make animals vulnerable to infections that may become zoonotic. However, it remains unclear whether the disruption to wildlife gut microbiomes is caused by habitat fragmentation per se or the combination of habitat fragmentation with additional anthropogenic disturbances, such as contact with humans, domesticated animals, invasive species, and their pathogens. Here, we show that habitat fragmentation per se does not impact the gut microbiome of a generalist rodent species native to Central America, Tome’s spiny rat Proechimys semispinosus, but additional anthropogenic disturbances do. Indeed, compared to protected continuous and fragmented forest landscapes that are largely untouched by other human activities, the gut microbiomes of spiny rats inhabiting human-disturbed fragmented landscapes revealed a reduced alpha diversity and a shifted and more dispersed beta diversity. Their microbiomes contained more taxa associated with domesticated animals and their potential pathogens, suggesting a shift in potential metagenome functions. On the one hand, the compositional shift could indicate a degree of gut microbial adaption known as metagenomic plasticity. On the other hand, the greater variation in community structure and reduced alpha diversity may signal a decline in beneficial microbial functions and illustrate that gut adaption may not catch up with anthropogenic disturbances, even in a generalist species with large phenotypic plasticity, with potentially harmful consequences to both wildlife and human health.
Highlights
In the Anthropocene, humans, domesticated animals, wildlife, and their environments are interconnected, especially as humans advance further into wildlife habitats
To test if habitat fragmentation per se or additional anthropogenic disturbance impacts the gut microbiome of a generalist species (Tome’s spiny rat) inhabiting lowland tropical rainforests in Central America (Supplementary Figs. 1 and 2), we first calculated the diversity of microbes within each of the 384 sampled individuals using three metrics: the observed number of amplicon sequence variants (ASVs), Shannon diversity, and Faith’s phylogenetic diversity (PD)
Using model selection based on the information-theoretic (IT) approach[24], we found very strong support for an effect of landscape on all three alpha diversity metrics: observed number of ASVs (ΔAICC = 19.63, R2GLMM(m) = 0.473, R2GLMM(c) = 0.579, Fig. 1a, Supplementary Data 1); Shannon diversity, in which alpha diversity is weighted for abundance (ΔAICC = 5.84, R2GLMM(m) = 0.150, R2GLMM(c) = 0.171, Fig. 1b, Supplementary Data 2); and Faith’s PD, which controls for phylogenetic relatedness (ΔAICC = 6.05, R2GLMM(m) = 0.438, R2GLMM(c) = 0.480, Supplementary Fig. 3, Supplementary Data 3)
Summary
In the Anthropocene, humans, domesticated animals, wildlife, and their environments are interconnected, especially as humans advance further into wildlife habitats. The three landscapes encompassed: (1) protected continuous tropical forests and (2) protected forested islands in the Panama Canal that allow us to study the effects of fragmentation on its own— both landscapes are largely undisturbed by human activities—and (3) nearby unprotected forested fragments embedded in an agricultural matrix that are subjected to further anthropogenic disturbances in addition to habitat fragmentation By comparing both protected landscapes to heavily human-disturbed, fragmented sites, our unique study design allowed us to, first, pick apart the effects of habitat fragmentation (i.e., habitat reduction and isolation) from those of additional anthropogenic disturbances (i.e., contact with humans, domesticated animals, invasive species, and pathogens within an agricultural matrix) on the gut microbiome and, second, to meticulously characterize the changes in gut community composition and metagenomic functional potential. Considering its integral role in host health, such a loss could be detrimental to wildlife health, but could promote microbial pathogens with zoonotic potential
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