The fine-scale landscape of immunity and parasitism in a wild ungulate population

Abstract

Spatial heterogeneity in parasite susceptibility and exposure is a common source of confounding variation in disease ecology studies. However, it is not known whether spatial autocorrelation acts on immunity in particular at small scales, within wild animal populations, and whether this predicts spatial patterns in infection. Here we used a well-mixed wild population of individually recognised red deer (Cervus elaphus) inhabiting a heterogeneous landscape to investigate fine-scale spatial patterns of immunity and parasitism. We noninvasively collected 842 faecal samples from 141 females with known ranging behaviour over two years. We quantified total and helminth-specific mucosal antibodies and counted propagules of three gastrointestinal helminth taxa. These data were analysed with linear mixed models using the Integrated Nested Laplace Approximation (INLA), using a Stochastic Partial Differentiation Equation approach (SPDE) to control for and quantify spatial autocorrelation.We also investigated whether spatial patterns of immunity and parasitism changed seasonally.We discovered substantial spatial heterogeneity in general and helminth-specific antibody levels and parasitism with two helminth taxa, all of which exhibited contrasting seasonal variation in their spatial patterns. Notably, strongyle nematode intensity did not align with density hotspots, while Fasciola hepatica intensity appeared to be strongly influenced by the presence of wet grazing. In addition, antibody hotspots did not correlate with distributions of any parasites. Our results suggest spatial heterogeneity may be an important factor affecting immunity and parasitism in a wide range of study systems. We discuss these findings with regards to the design of sampling regimes and public health interventions, and suggest that disease ecology studies investigate spatial heterogeneity more regularly to enhance their results, even when examining small geographic areas.

Macroimmunology: The drivers and consequences of spatial patterns in wildlife immune defence

“…Correlograms often show a linear or exponential decline with increasing distance, suggesting a highly localized spatial mechanism. Recent work on red deer Cervus elaphus illustrates such fine‐scale autocorrelation and suggests that environmental processes can shape defence within even an individual's home range (Albery, Becker, Kenyon, Nussey, & Pemberton, ). In contrast, correlograms applied to vampire bat leukocytes demonstrated autocorrelation at broad scales (thousands of kilometres), suggesting that conditions of the latitudinal range margins were more important determinants of immunity than local predictors (Becker, Nachtmann, et al, ).…”

“…INLA incorporates a two‐dimensional spatial random effect that can be plotted to investigate hot‐ and cold spots of immunity. One INLA case study highlighted spatial agreement and discordance between several immune metrics and parasitism in red deer (Albery et al, ). Greater adoption of spatial statistics will strengthen our understanding of how the environment shapes immune defence while minimizing potential statistical artefacts.…”

“…Considering this joint variation, spatial patterns in immunity could be most evident in seasons when food is limited or when abiotic conditions are harsh (Nelson & Demas, ). For example, work on red deer immunity found that spatial patterns in antibody concentrations varied substantially across seasons (Albery et al, ).…”