Agricultural Fast Food: Bats Feeding in Banana Monocultures Are Heavier but Have Less Diverse Gut Microbiota

Abstract

Habitat alteration for agriculture can negatively affect wildlife physiology and health by decreasing diet diversity and increasing exposure to agrochemicals for animals foraging in altered landscapes. Such negative effects may be mediated by the disruption of the gut microbiota (termed dysbiosis), yet evidence for associations between habitat alteration, wildlife health, and the gut microbiota remains scarce. We examine the association between management intensity of banana plantations and both the body condition and gut microbiota composition of nectar-feeding bats Glossophaga soricina, which commonly forage within banana plantations across Latin America. We captured and measured 196 bats across conventional monocultures, organic plantations, and natural forests in Costa Rica, and quantified gut microbiome bacterial phylogenetic diversity using 16S rRNA amplicon sequencing. We found that gut microbiota from bats foraging in conventional monocultures were overall less phylogenetically diverse than those from bats foraging in organic plantations or natural forests, both of which were characterized by diverse bacterial assemblages and individualized microbiota. Despite lower diversity, co-occurrence network complexity was higher in conventional monocultures, potentially indicating altered microbial interactions in agricultural landscapes. Bats from both organic and conventional plantations tended to be larger and heavier than their forest counterparts, reflecting the higher food supply. Overall, our study reveals that whilst both conventional monocultures and organic plantations provide a reliable food source for bats, conventional monocultures are associated with less diverse and potentially dysbiotic microbiota, whilst organic plantations promote diverse and individualized gut microbiota akin to their natural forest-foraging counterparts. Whilst the long-term negative effects of anthropogenically-altered microbiota are unclear, our study provides further evidence from a novel perspective that organic agricultural practices are beneficial for wildlife health.

The fecal bacterial microbiome of the Kuhl’s pipistrelle bat (Pipistrellus kuhlii) reflects landscape anthropogenic pressure

“…The family Alcaligenaceae has been described in the fecal microbiome of different bat species [ 24 , 25 , 88 ], regardless of their dietary habits or geographic distribution. Furthermore, this family of proteobacteria was found to be characteristic of Palla’s Long-tongued bats ( Glossophaga soricine ) foraging in natural forests in comparison to those foraging in organic or conventional banana monocultures where pesticides were used [ 43 ]. As a highly diverse bacterial linage, further research is needed to understand Alcaligenaceae ’s functional significance in the gut microbiome of bats.…”

“…Their impact on the nutrient cycling of soil and its microbes further affects the food webs of ecosystems [ 40 , 41 ], which eventually may alter the intestinal microbiome of animals. However, evidence for an association between habitat degradation and gut microbiota changes in bat species has barely been explored [ 42 , 43 ]. Furthermore, information on bat microbial communities -especially these detected in feces- and their role in bat’s health remain scarce.…”

Edge effects and vertical stratification of aerial insectivorous bats across the interface of primary-secondary Amazonian rainforest

“…Whilst we did not detect many direct changes in bat activity in response to edges, the deviation we observed from typical stratum use may reflect the potential for more subtle effects on bat populations. Habitat disturbance, including edge effects, can affect a species' behaviour, physiology, and other fitness parameters [8,11,81,82]. At least two Amazonian phyllostomids change their habitat preferences to utilize more strata in forest fragments than in continuous forest when locating prey [45].…”

“…However, more research is needed to test this hypothesis. Habitat deterioration can also reduce the richness of prey in insectivorous bat diets in disturbed habitats and the long-term impacts of this are not yet fully understood [81,82]. Similarly, Estrada-Villegas et al [73] showed fragmentation increased the activity of aerial insectivorous forest bats and altered their assemblage composition.…”

Disentangling direct from indirect effects of habitat disturbance on multiple components of biodiversity

“…At the same time, parasites maintain genetic diversity (Cabalzar et al, 2019) and even drive host speciation (Bordes & Morand, 2008;Eizaguirre et al, 2012). Similarly, the environment (Alpízar et al, 2021;Fackelmann et al, 2021;Ruiz-Calderon et al, 2016) and host genetics (Grieneisen et al, 2021;Morella et al, 2020;Suzuki et al, 2019), as well as pathogenic infections (Sabey et al, 2021;Wasimuddin et al, 2019) determine the composition of the commensal microbiome. The gut microbiome itself can modulate host immunity and, thus, parasite or pathogen resistance (Armenteros et al, 2015;Brestoff & Artis, 2013;Näpflin & Schmid-Hempel, 2018).…”