skip to main content


Title: 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 andBartonellaspp. 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 inPteronotus mesoamericanusandDermanura phaeotis. ForBartonellaspp., mercury was associated with particularly low odds of infection in the genusPteronotusbut 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.

 
more » « less
Award ID(s):
1716698
NSF-PAR ID:
10452801
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;  ;
Publisher / Repository:
Wiley-Blackwell
Date Published:
Journal Name:
Journal of Applied Ecology
Volume:
58
Issue:
4
ISSN:
0021-8901
Page Range / eLocation ID:
p. 879-889
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract

    Monitoring the health of wildlife populations is essential in the face of increased agricultural expansion and forest fragmentation. Loss of habitat and habitat degradation can negatively affect an animal’s physiological state, possibly resulting in immunosuppression and increased morbidity or mortality. We sought to determine how land conversion may differentially impact cellular immunity and infection risk in Neotropical bats species regularly infected with bloodborne pathogens, and to evaluate how effects may vary over time and by dietary habit. We studied common vampire bats (Desmodus rotundus), northern yellow-shouldered bats (Sturnira parvidens) and Mesoamerican mustached bats (Pteronotus mesoamericanus), representing the dietary habits of sanguivory, frugivory and insectivory respectively, in northern Belize. We compared estimated total white blood cell count, leukocyte differentials, neutrophil to lymphocyte ratio and infection status with two bloodborne bacterial pathogens (Bartonella spp. and hemoplasmas) of 118 bats captured in a broadleaf, secondary forest over three years (2017–2019). During this period, tree cover decreased by 14.5% while rangeland expanded by 14.3%, indicating increasing habitat loss and fragmentation. We found evidence for bat species-specific responses of cellular immunity between years, with neutrophil counts significantly decreasing in S. parvidens from 2017 to 2018, but marginally increasing in D. rotundus. However, the odds of infection with Bartonella spp. and hemoplasmas between 2017 and 2019 did not differ between bat species, contrary to our prediction that pathogen prevalence may increase with land conversion. We conclude that each bat species invested differently in cellular immunity in ways that changed over years of increasing habitat loss and fragmentation. We recommend further research on the interactions between land conversion, immunity and infection across dietary habits of Neotropical bats for informed management and conservation.

     
    more » « less
  2. Abstract

    The spatial organization of populations determines their pathogen dynamics. This is particularly important for communally roosting species, whose aggregations are often driven by the spatial structure of their environment.

    We develop a spatially explicit model for virus transmission within roosts of Australian tree‐dwelling bats (Pteropusspp.), parameterized to reflect Hendra virus. The spatial structure of roosts mirrors three study sites, and viral transmission between groups of bats in trees was modelled as a function of distance between roost trees. Using three levels of tree density to reflect anthropogenic changes in bat habitats, we investigate the potential effects of recent ecological shifts in Australia on the dynamics of zoonotic viruses in reservoir hosts.

    We show that simulated infection dynamics in spatially structured roosts differ from that of mean‐field models for equivalently sized populations, highlighting the importance of spatial structure in disease models of gregarious taxa. Under contrasting scenarios of flying‐fox roosting structures, sparse stand structures (with fewer trees but more bats per tree) generate higher probabilities of successful outbreaks, larger and faster epidemics, and shorter virus extinction times, compared to intermediate and dense stand structures with more trees but fewer bats per tree. These observations are consistent with the greater force of infection generated by structured populations with less numerous but larger infected groups, and may flag an increased risk of pathogen spillover from these increasingly abundant roost types.

    Outputs from our models contribute insights into the spread of viruses in structured animal populations, like communally roosting species, as well as specific insights into Hendra virus infection dynamics and spillover risk in a situation of changing host ecology. These insights will be relevant for modelling other zoonotic viruses in wildlife reservoir hosts in response to habitat modification and changing populations, including coronaviruses like SARS‐CoV‐2.

     
    more » « less
  3. Abstract

    Models of host–pathogen interactions help to explain infection dynamics in wildlife populations and to predict and mitigate the risk of zoonotic spillover. Insights from models inherently depend on the way contacts between hosts are modelled, and crucially, how transmission scales with animal density.

    Bats are important reservoirs of zoonotic disease and are among the most gregarious of all mammals. Their population structures can be highly heterogeneous, underpinned by ecological processes across different scales, complicating assumptions regarding the nature of contacts and transmission. Although models commonly parameterise transmission using metrics of total abundance, whether this is an ecologically representative approximation of host–pathogen interactions is not routinely evaluated.

    We collected a 13‐month dataset of tree‐roostingPteropusspp. from 2,522 spatially referenced trees across eight roosts to empirically evaluate the relationship between total roost abundance and tree‐level measures of abundance and density—the scale most likely to be relevant for virus transmission. We also evaluate whether roost features at different scales (roost level, subplot level, tree level) are predictive of these local density dynamics.

    Roost‐level features were not representative of tree‐level abundance (bats per tree) or tree‐level density (bats per m2or m3), with roost‐level models explaining minimal variation in tree‐level measures. Total roost abundance itself was either not a significant predictor (tree‐level 3D density) or only weakly predictive (tree‐level abundance).

    This indicates that basic measures, such as total abundance of bats in a roost, may not provide adequate approximations for population dynamics at scales relevant for transmission, and that alternative measures are needed to compare transmission potential between roosts. From the best candidate models, the strongest predictor of local population structure was tree density within roosts, where roosts with low tree density had a higher abundance but lower density of bats (more spacing between bats) per tree.

    Together, these data highlight unpredictable and counterintuitive relationships between total abundance and local density. More nuanced modelling of transmission, spread and spillover from bats likely requires alternative approaches to integrating contact structure in host–pathogen models, rather than simply modifying the transmission function.

     
    more » « less
  4. Abstract

    Host ecological factors and external environmental factors are known to influence the structure of gut microbial communities, but few studies have examined the impacts of environmental changes on microbiotas in free‐ranging animals. Rapid land‐use change has the potential to shift gut microbial communities in wildlife through exposure to novel bacteria and/or by changing the availability or quality of local food resources. The consequences of such changes to host health and fitness remain unknown and may have important implications for pathogen spillover between humans and wildlife. To better understand the consequences of land‐use change on wildlife microbiotas, we analyzed long‐term dietary trends, gut microbiota composition, and innate immune function in common vampire bats (Desmodus rotundus) in two nearby sites in Belize that vary in landscape structure. We found that vampire bats living in a small forest fragment had more homogenous diets indicative of feeding on livestock and shifts in microbiota heterogeneity, but not overall composition, compared to those living in an intact forest reserve. We also found that irrespective of sampling site, vampire bats which consumed relatively more livestock showed shifts in some core bacteria compared with vampire bats which consumed relatively less livestock. The relative abundance of some core microbiota members was associated with innate immune function, suggesting that future research should consider the role of the host microbiota in immune defense and its relationship to zoonotic infection dynamics. We suggest that subsequent homogenization of diet and habitat loss through livestock rearing in the Neotropics may lead to disruption to the microbiota that could have downstream impacts on host immunity and cross‐species pathogen transmission.

     
    more » « less
  5. Abstract

    Emerging infectious diseases have caused population declines and biodiversity loss. The ability of pathogens to survive in the environment, independent of their host, can exacerbate disease impacts and increase the likelihood of species extinction. Control of pathogens with environmental stages remains a significant challenge for conservation and effective management strategies are urgently needed.

    We examined the effectiveness of managing environmental exposure to reduce the impacts of an emerging infectious disease of bats, white‐nose syndrome (WNS). We used a chemical disinfectant, chlorine dioxide (ClO2), to experimentally reducePseudogymnoascus destructans, the fungal pathogen causing WNS, in the environment. We combined laboratory experiments with 3 years of field trials at four abandoned mines to determine whether ClO2could effectively removeP. destructansfrom the environment, reduce host infection and limit population impacts.

    ClO2was effective at killingP. destructansin vitro across multiple concentrations. In field settings, higher concentrations of ClO2treatment were needed to sufficiently reduce viableP. destructansconidia in the environment.

    The reduction in the environmental reservoir at treatment sites resulted in lower fungal loads on bats compared to untreated control populations. Survival following treatment was also higher in little brown bats (Myotis lucifugus), and trended higher for tricolored bats (Perimyotis subflavus).

    Synthesis and applications. Our results highlight that targeted management of sources for environmental transmission can be an effective control strategy for wildlife disease. We found that successfully reducing pathogen in the environment decreased disease severity and increased survival, but required higher treatment exposure than was effective in laboratory experiments, and the effects varied among species. More broadly, our findings have implications for other emerging wildlife diseases with free‐living pathogen stages by highlighting how the degree of environmental contamination can have cascading impacts on hosts, presenting an opportunity for intervention.

     
    more » « less