Long-term temporal trends in gastrointestinal parasite infection in wild Soay sheep

Abstract

Monitoring the prevalence and abundance of parasites over time is important for addressing their potential impact on host life histories, immunological profiles and their influence as a selective force. Only long-term ecological studies have the potential to shed light on both the temporal trends in infection prevalence and abundance and the drivers of such trends, because of their ability to dissect drivers that may be confounded over shorter time scales. Despite this, only a relatively small number of such studies exist. Here, we analysed changes in the prevalence and abundance of gastrointestinal parasites in the wild Soay sheep population of St. Kilda across 31 years. The host population density (PD) has increased across the study, and PD is known to increase parasite transmission, but we found that PD and year explained temporal variation in parasite prevalence and abundance independently. Prevalence of both strongyle nematodes and coccidian microparasites increased during the study, and this effect varied between lambs, yearlings and adults. Meanwhile, abundance of strongyles was more strongly linked to host PD than to temporal (yearly) dynamics, while abundance of coccidia showed a strong temporal trend without any influence of PD. Strikingly, coccidian abundance increased 3-fold across the course of the study in lambs, while increases in yearlings and adults were negligible. Our decades-long, intensive, individual-based study will enable the role of environmental change and selection pressures in driving these dynamics to be determined, potentially providing unparalleled insight into the drivers of temporal variation in parasite dynamics in the wild.

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.…”

“…The wild Soay sheep ( Ovis aries ) of St Kilda have been studied since 1985, with individual-based measurements of behaviour, life history, and parasitism throughout this time [24]. They host a diversity of gastrointestinal parasites, all of which have some environmental phase in between hosts and achieve reinfection through reingestion [25,26]. They also host sheep keds ( Melophagus ovinus ): wingless ectoparasitic flies that achieve transmission through direct contact [27].…”

“…This mechanism has been linked with greater parasite infection in lambs in high-density years [25,29], and is thought to regulate the population by driving worse condition and greater mortality in these years [26]. Nevertheless, the remaining parasites in the population have yet to be successfully linked with population density [25], and strongyles have not been linked with within-year density metrics or aligned with spatial host distributions; rather, all density analyses have been carried out by linking total population size with infection in a given year, with only one density value applied across the population per year [26]. 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.…”

“…Strongyle infection dynamics in the sheep are broadly thought to be driven by population density, where high numbers of grazing sheep produce larger numbers of infectious larvae to be ingested, which then results in greater exposure and therefore greater infection [26]. This mechanism has been linked with greater parasite infection in lambs in high-density years [25,29], and is thought to regulate the population by driving worse condition and greater mortality in these years [26]. Nevertheless, the remaining parasites in the population have yet to be successfully linked with population density [25], and strongyles have not been linked with within-year density metrics or aligned with spatial host distributions; rather, all density analyses have been carried out by linking total population size with infection in a given year, with only one density value applied across the population per year [26].…”

Helminth parasites of the wood mouse Apodemus sylvaticus in Southern England: levels of infection, species richness and interactions between species

“…Seasonal changes in helminth burdens are also well recognized, although most such studies have been conducted over very short time spans, usually just 1–2 years (Lewis, 1968; Langley & Fairley, 1982; O'Sullivan et al , 1984; Montgomery & Montgomery, 1988, 1989, 1990; Gregory, 1992; Abu-Madi et al , 1998, 2000; Behnke et al , 1999). More recently, attention has shifted to perturbation experiments in wild mice (Ferrari et al , 2004; Pederson & Grieves, 2008; Knowles et al , 2013; Pederson & Antonovics, 2013) and to monitoring long-term changes (Grzybek et al, 2015a: Behnke et al , 2019, 2021; Sweeny et al , 2021a; Hayward et al , 2022; Wood et al , 2023) Both approaches have revealed remarkable stability of some helminth species, usually the core species, as well as marked fluctuations in others reflecting between year cycles and responses to perturbation, temporally declining worm burdens, as well as complete loss and acquisition of new species.…”