Seasonality of helminth infection in wild red deer varies between individuals and between parasite taxa

Abstract

Parasitism in wild mammals can vary according to myriad intrinsic and extrinsic factors, many of which vary seasonally. However, seasonal variation in parasitism is rarely studied using repeated samples from known individuals. Here we used a wild population of individually recognized red deer (Cervus elaphus) on the Isle of Rum to quantify seasonality and intrinsic factors affecting gastrointestinal helminth parasitism over the course of a year. We collected 1020 non-invasive faecal samples from 328 known individuals which we then analysed for propagules of three helminth taxa: strongyle nematodes, the common liver fluke Fasciola hepatica and the tissue nematode Elaphostrongylus cervi. Zero-inflated Poisson models were used to investigate how season, age and sex were associated with parasite prevalence and count intensity, while Poisson models were used to quantify individual repeatability within and between sampling seasons. Parasite intensity and prevalence varied according to all investigated factors, with opposing seasonality, age profiles and sex biases between parasite taxa. Repeatability was moderate, decreased between seasons and varied between parasites; both F. hepatica and E. cervi showed significant between-season repeatability, while strongyle nematode counts were only repeatable within-season and showed no repeatability within individuals across the year.

Fitness costs of parasites explain multiple life history tradeoffs in a wild mammal

“…Strongyles are ubiquitous ruminant parasites that are present at high prevalence in this population and which increase in intensity in lactating individuals (Albery et al ., 2018b). Previous studies in this population have also examined the helminths Elaphostrongylus cervi and Fasciola hepatica (Albery et al ., 2018a; b). We chose to examine strongyles but not E. cervi or F. hepatica for several reasons: we did not want to add too many links to the DAG for reasons of interpretability; strongyles are most expected to have strong fitness costs (Hoberg et al ., 2001) and exhibited the most profound reproductive tradeoff in terms of significance and magnitude (Albery et al ., 2018b)a; we did not expect E. cervi to have strong fitness effects (Irvine et al ., 2006); and F. hepatica is present at relatively low prevalence in adult females, preventing it from being fitted easily as an explanatory variable (Albery et al ., 2018a).…”

“…We also assayed faecal samples collected in November (e.g. Albery et al ., 2018a). However, females exhibited very low strongyle prevalence in the autumn compared with spring and summer, preventing our FEC data from approximating normality and providing little variation to test when fitted as an explanatory variable.…”

“…Females that give birth to a calf that dies within the first few months of its life have similar fitness outcomes to those that do not give birth, implying that gestation has a minimal cost relative to lactation (Clutton-Brock et al ., 1989). The deer are infected with several helminth parasites, with decreased mucosal IgA levels and increased parasite intensity in reproductive females (Albery et al ., 2018a; b). Lactation but not gestation results in substantially increased parasite counts, partially reflecting the cost of reproduction for fitness; however, investment in gestation results in decreased mucosal IgA levels (Albery et al ., 2018b).…”

Seasonal dietary shifts enhance parasite transmission to lake salmonids during ice cover

“…Seasonal changes in the availability of intermediate hosts and infective stages may produce distinct seasonal patterns in parasite transmission (Esch & Fernández, 1993; Thieltges, Jensen, & Poulin, 2008), consequently affecting the parasite community structure and dynamics over the annual cycle. For instance, spring and summer, as opposed to winter, often correspond with a peak of helminth egg output and increased intensity of infections in wild Red deer populations from temperate regions (Albery et al, 2018). Such seasonal trends in parasite transmission are, however, not universal, as exemplified by the transmission of the nematode Marshallagia marshalli to reindeer in the high Arctic (Svalbard) which occurs throughout the winter months despite extreme cold conditions (Carlsson et al, 2012).…”

Habitat and host factors associated with liver fluke (Fasciola hepatica) diagnoses in wild red deer (Cervus elaphus) in the Scottish Highlands

“…This is in excess of the limitations proposed by Ollerenshaw [15], beyond which the relationship between weather and incidence ceases to be valid. Fasciola hepatica prevalence in red deer varies temporally [16] and geographically throughout the Highlands [17]. While geographical variation could be related to F. hepatica development in certain areas of the Scottish Highlands being limited by temperature [18], the landscape is markedly different from the pasture dominated rural areas of England and Wales in which temperature-moisture relationships were originally validated.…”