Predictors and immunological correlates of sublethal mercury exposure in vampire bats

Abstract

Mercury (Hg) is a pervasive heavy metal that often enters the environment from anthropogenic sources such as gold mining and agriculture. Chronic exposure to Hg can impair immune function, reducing the ability of animals to resist or recover from infections. How Hg influences immunity and susceptibility remains unknown for bats, which appear immunologically distinct from other mammals and are reservoir hosts of many pathogens of importance to human and animal health. We here quantify total Hg (THg) in hair collected from common vampire bats (Desmodus rotundus), which feed on blood and are the main reservoir hosts of rabies virus in Latin America. We examine how diet, sampling site and year, and bat demography influence THg and test the consequences of this variation for eight immune measures. In two populations from Belize, THg concentrations in bats were best explained by an interaction between long-term diet inferred from stable isotopes and year. Bats that foraged more consistently on domestic animals exhibited higher THg. However, relationships between diet and THg were evident only in 2015 but not in 2014, which could reflect recent environmental perturbations associated with agriculture. THg concentrations were low relative to values previously observed in other bat species but still correlated with bat immunity. Bats with higher THg had more neutrophils, weaker bacterial killing ability and impaired innate immunity. These patterns suggest that temporal variation in Hg exposure may impair bat innate immunity and increase susceptibility to pathogens such as bacteria. Unexpected associations between low-level Hg exposure and immune function underscore the need to better understand the environmental sources of Hg exposure in bats and the consequences for bat immunity and susceptibility.

Keywords: Chiroptera; agriculture; ecoimmunology; ecotoxicology; spatio-temporal; wildlife health.

Figure 1.

(a) Sampling locations of vampire bats and potential prey in Orange Walk District, Belize. Points show the sample location and type (bat and type of prey) in four sites (K, Ka'Kabish; I, Indian Church Village; L, LAR; P, Pacbitun). Grey shading denotes cattle density (per square kilometre) from the Food and Agriculture Organization estimates in each 5 km cell. Polygons display main ecosystem classifications from the Biodiversity and Environmental Resource Data System of Belize, with transparent regions corresponding to agricultural habitat. (b) Uncorrected means and standard deviation of δ¹³C and δ¹⁵N for wild (green diamond) and domestic (livestock and poultry; brown triangle) prey categories. Coloured symbols indicate individual prey isotope values with colours corresponding to prey group (domestic versus wild) and shapes corresponding to species. Circles are isotope values for individual bats (white, LAR; black, Ka'Kabish).

Figure 2.

Relationships between year, bat diet and hair THg for the top-supported linear models. Solid lines show the fitted values, and dashed lines show THg thresholds of 1 mg kg⁻¹ and 10 mg kg⁻¹. THg values are shown on a log scale.

Figure 3.

Univariate tests of the relationship between hair THg and immune parameters (absolute leucocyte counts, NL ratios, BKA, IgG OD). Solid lines indicate statistically significant fits from generalized linear models, linear regressions or variable dispersion beta regression. Dashed lines show fits from models with suggestive associations but non-significant effects after adjustment for multiple comparisons (p < 0.15). THg values are shown on a log scale. Bats sampled in 2014 are shown in grey and those sampled in 2015 are shown in black.

Figure 4.

Multivariate analysis of associations between hair THg and bat immune profiles. (a) Biplot of the first two PCs on seven measures of immune function, with arrows indicating PC loadings and points scaled by THg. (b,c) Linear relationships between THg and the first two PCs, with the dotted line showing model fit after outlier removal. THg values are shown on a log scale. Bats sampled in 2014 are shown in grey and those sampled in 2015 are shown in black.