Age‐specific impacts of vegetation functional traits on gastrointestinal nematode parasite burdens in a large herbivore

Abstract

Gastrointestinal nematode (GIN) parasites play an important role in the ecological dynamics of many animal populations. Recent studies suggest that fine‐scale spatial variation in GIN infection dynamics is important in wildlife systems, but the environmental drivers underlying this variation remain poorly understood. We used data from over two decades of GIN parasite egg counts, host space use, and spatial vegetation data from a long‐term study of Soay sheep on St Kilda to test how spatial autocorrelation and vegetation in an individual's home range predict parasite burden across three age groups. We developed a novel approach to quantify the plant functional traits present in a home range to describe the quality of vegetation present. Effects of vegetation and space varied between age classes. In immature lambs, strongyle parasite faecal egg counts (FEC) were spatially structured, being highest in the north and south of our study area. Independent of host body weight and spatial autocorrelation, plant functional traits predicted parasite egg counts. Higher egg counts were associated with more digestible and preferred plant functional traits, suggesting the association could be driven by host density and habitat preference. In contrast, we found no evidence that parasite FEC were related to plant functional traits in the host home range in yearlings or adult sheep. Adult FEC were spatially structured, with highest burdens in the north‐east of our study area, while yearling FEC showed no evidence of spatial structuring. Parasite burdens in immature individuals appear more readily influenced by fine‐scale spatial variation in the environment, highlighting the importance of such heterogeneity for our understanding of wildlife epidemiology and health. Our findings support the importance of fine‐scale environmental variation for wildlife disease ecology and provides new evidence that such effects may vary across demographic groups within a population.

Local and global density have distinct and parasite-dependent effects on infection in wild sheep

“…Population density likely drives greater helminth infection by driving greater indirect contact: that is, if more individuals are inhabiting and shedding parasites in higher-density areas, the parasites will achieve a higher concentration on the pasture, thereby driving greater individual-level exposure in these areas. This corroborates prior knowledge concerning the role of population density in driving infection in this population via greater environmental exposure [25,26] – and offers an explanation for the previously observed positive correlation between strongyle count in lambs and preferred vegetation, which is likely to coincide with areas of high host density [30]. However, our use of individual-level (spatial) density metrics allowed us to pick up much finer-scale relationships between density and infection, and thereby detected several more such relationships than previous studies.…”

“…Alternatively, a similar pattern could arise because young individuals are particularly vulnerable to stresses associated with higher density like greater resource competition, reducing their immune resistance and therefore driving greater parasite count [19]. This may be supported by the previously observed positive correlation between strongyle count in lambs and high-quality vegetation, which is likely to coincide with areas of high host density [30]. Alternatively, age-related differences in density-infection patterns could arise through demographic processes linked to those described above: in higher-density areas, heavily infected lambs may die more quickly, leaving behind more resistant lambs and therefore producing a less positive relationship between density and infection at the population level in older individuals (i.e.…”

“…In addition, compared to other parasites, coccidia may be more strongly linked to reduced condition in higher-density areas across all host groups, or their transmission could be more efficient in areas of higher density due to vegetation composition or microclimate, for example. The fitness and condition impacts of coccidia have only been rarely examined in this population [43], but we may be able to interrogate these mechanisms in the future – particularly if combined with analyses of vegetation composition and socio-spatial behaviour [30]. Altogether, the role of coccidia in density dependent regulation of this population could be stronger than previously anticipated.…”

“…As such, it remains to be seen how strongyles are driven by density on finer spatiotemporal scales, and whether the density trends are ubiquitous or specific to strongyles. Notably, a previous study found a strong positive correlation between vegetation quality and strongyle count in lambs, which we asserted could be linked to greater density in higher-quality areas [30].…”

“…via structural equation modelling, which has previously shown that parasites regulate individual reproductive fitness in a similar way in this population [28]. They could further examine whether density-infection relationships depend on resource availability, which should be reduced in higher-density areas and years in this population; this combined exacerbation of exposure and susceptibility will likely exponentially influence parasite count and disproportionately limit the population’s size and density [26,30].…”