Disentangling interactions among mercury, immunity and infection in a Neotropical bat community

Abstract

Contaminants such as mercury are pervasive and can have immunosuppressive effects on wildlife. Impaired immunity could be important for forecasting pathogen spillover, as many land‐use changes that generate mercury contamination also bring wildlife into close contact with humans and domestic animals. However, the interactions among contaminants, immunity and infection are difficult to study in natural systems, and empirical tests of possible directional relationships remain rare. We capitalized on extreme mercury variation in a diverse bat community in Belize to test association among contaminants, immunity and infection. By comparing a previous dataset of bats sampled in 2014 with new data from 2017, representing a period of rapid agricultural land conversion, we first confirmed bat species more reliant on aquatic prey had higher fur mercury. Bats in the agricultural habitat also had higher mercury in recent years. We then tested covariation between mercury and cellular immunity and determined if such relationships mediated associations between mercury and bacterial pathogens. As bat ecology can dictate exposure to mercury and pathogens, we also assessed species‐specific patterns in mercury–infection relationships. Across the bat community, individuals with higher mercury had fewer neutrophils but not lymphocytes, suggesting stronger associations with innate immunity. However, the odds of infection for haemoplasmas and Bartonella spp. were generally lowest in bats with high mercury, and relationships between mercury and immunity did not mediate infection patterns. Mercury also showed species‐ and clade‐specific relationships with infection, being associated with especially low odds for haemoplasmas in Pteronotus mesoamericanus and Dermanura phaeotis. For Bartonella spp., mercury was associated with particularly low odds of infection in the genus Pteronotus but high odds in the subfamily Stenodermatinae. Synthesis and application. Lower general infection risk in bats with high mercury despite weaker innate defense suggests contaminant‐driven loss of pathogen habitat (i.e. anemia) or vector mortality as possible causes. Greater attention to these potential pathways could help disentangle relationships among contaminants, immunity and infection in anthropogenic habitats and help forecast disease risks. Our results also suggest that contaminants may increase infection risk in some taxa but not others, emphasizing the importance of considering surveillance and management at different phylogenetic scales.

Avian influenza antibody prevalence increases with mercury contamination in wild waterfowl

“…The increase in antibody detection associated with mercury was as large as some species-specific differences in influenza prevalence [17,18], suggesting that contaminant-induced susceptibility to pathogens could be a major contributor to differences in infection prevalence across species. Moreover, we observed these relationships at relatively low mercury concentrations, consistent with a prior study of bat immune function [38], and suggesting that infection risk might be relatively sensitive to contaminant exposure. In addition, although we found no association between infection and body condition, environmental contaminants might have more significant population impacts when interacting with more virulent and emerging pathogens.…”

“…MeHg can also alter immune function in mammals and birds [37], including compromising both the innate immune response (e.g. inflammation [9,[38][39][40][41]) and the adaptive immune response (e.g. lymphocyte production [38,42,43], antibody titres [10]).…”

“…inflammation [9,[38][39][40][41]) and the adaptive immune response (e.g. lymphocyte production [38,42,43], antibody titres [10]). Both innate and adaptive immunity influence the probability and severity of influenza infection [44,45], so mercury contamination could affect the prevalence of influenza infection and its impacts waterfowl populations.…”

Body size affects immune cell proportions in birds and non-volant mammals, but not bats

“…During April and May in 2017 and 2018, we sampled 160 bats from 26 species in the Orange Walk District of Belize (Herrera et al, 2018;Becker et al, 2020aBecker et al, , 2021. Bats were captured using mist nets (monitored continuously from approximately 19:00 h to 22:00 h) and harp traps (monitored every half-hour from 18:00 h to 22:00 h and then at 05:00 h the following morning); all individuals were identified to species based on morphology (Reid, 1997).…”

Impacts of nickel mining on the DNA and hematological parameters of two species of bat in central Brazil

“…The cell counts recorded in the present study are consistent with the ndings of previous studies of freeliving bats(Santos et al 2007). Continuous exposure to heavy metals can lead to immunosuppression in wild animals, which increases the vulnerability of the organism to contamination by pathogens(Grasman, 2002;Becker et al 2021). In a studyof sh exposed to nickel contamination, Marenkov et al…”