Dietary niche breadth influences the effects of urbanization on the gut microbiota of sympatric rodents

Abstract

Cities are among the most extreme forms of anthropogenic ecosystem modification, and urbanization processes exert profound effects on animal populations through multiple ecological pathways. Increased access to human‐associated food items may alter species' foraging behavior and diet, in turn modifying the normal microbial community of the gastrointestinal tract (GIT), ultimately impacting their health. It is crucial we understand the role of dietary niche breadth and the resulting shift in the gut microbiota as urban animals navigate novel dietary resources. We combined stable isotope analysis of hair and microbiome analysis of four gut regions across the GIT to investigate the effects of urbanization on the diet and gut microbiota of two sympatric species of rodents with different dietary niches: the omnivorous large Japanese field mouse (Apodemus speciosus) and the relatively more herbivorous gray red‐backed vole (Myodes rufocanus). Both species exhibited an expanded dietary niche width within the urban areas potentially attributable to novel anthropogenic foods and altered resource availability. We detected a dietary shift in which urban A. speciosus consumed more terrestrial animal protein and M. rufocanus more plant leaves and stems. Such changes in resource use may be associated with an altered gut microbial community structure. There was an increased abundance of the presumably probiotic Lactobacillus in the small intestine of urban A. speciosus and potentially pathogenic Helicobacter in the colon of M. rufocanus. Together, these results suggest that even taxonomically similar species may exhibit divergent responses to urbanization with consequences for the gut microbiota and broader ecological interactions.

Microbiome diversity and zoonotic bacterial pathogen prevalence in Peromyscus mice from agricultural landscapes and synanthropic habitat

“…Shifts in microbiome composition are commonly found in wildlife species when comparing individuals in native and anthropogenic environments (Diaz et al., 2023; Murray et al., 2020). These shifts could be attributed to dietary shifts based on habitat type and food availability, particularly in anthropogenic environments (Anders et al., 2022). Microbiome shifts in anthropogenic environments can also signal plasticity in the gut microbiome that may be allowing individuals to adapt to novel environments and new food sources (Littleford‐Colquhoun et al., 2019).…”

“…Wildlife living in close proximity to humans commonly experience changes to the composition of their microbiome compared to counterparts in native habitat (Anders et al, 2022;Berlow et al, 2021).…”

“…The gut microbiome plays a role in host health (Marchesi et al., 2016) and immune function (Schluter et al., 2020), and disruption of the normal microbiome, or dysbiosis, has been linked to various health conditions in wildlife, livestock, and domestic animals (Funosas et al., 2021; Monteiro & Faciola, 2020; Suchodolski, 2022). Wildlife living in close proximity to humans commonly experience changes to the composition of their microbiome compared to counterparts in native habitat (Anders et al., 2022; Berlow et al., 2021). Often, wildlife in anthropogenic environments exhibit lower microbiome diversity (Amato et al., 2013; Fackelmann et al., 2021), potentially due to a shift towards lower‐quality food or a lower diversity of food resources (Fuirst et al., 2018; Teyssier et al., 2020).…”

Effects of past and present habitat on the gut microbiota of a wild rodent

“…Moreover, maternal transmission [12] and social contact [13] can also impact the gut microbiota composition, although the influence of the maternal microbiota apparently weakens with age [12,14]. Thus, a typical feature of the animal gut microbiota is that conspecifics have distinct communities depending on where they live [11,15]. When an animal moves to a new environment, it is reasonable to expect a concomitant change in the gut microbiota, for example as a response to new resources [16][17][18] or contact with new conspecifics and/or pathogens.…”

“…present habitat) on the gut microbiota composition by performing an RT experiment with adult wild rodents and their newborn offspring (the bank vole, Clethrionomys glareolus; formerly Myodes glareolus; [39]) inhabiting contrasting (urban and rural) forest habitats. We chose this model system since both environmental [40] and host-associated [15,41] microbiota differ between urban and rural forests, thus allowing us to detect flexibility and resistance after translocation. In line with previous RT studies [31][32][33], we hypothesized that (1) the adult posttransfer gut microbiota will be explained more by the contemporary environment than by the prior environment.…”