Even though theoretical models show that parasites may regulate host population densities, few empirical studies have given support to this hypothesis. We present experimental and observational evidence for a host-parasite interaction where the parasite has sufficient impact on host population dynamics for regulation to occur. During a six year study of the Svalbard reindeer and its parasitic gastrointestinal nematode Ostertagia gruehneri we found that anthelminthic treatment in April-May increased the probability of a reindeer having a calf in the next year, compared with untreated controls. However, treatment did not influence the over-winter survival of the reindeer. The annual variation in the degree to which parasites depressed fecundity was positively related to the abundance of O. gruehneri infection the previous October, which in turn was related to host density two years earlier. In addition to the treatment effect, there was a strong negative effect of winter precipitation on the probability of female reindeer having a calf. A simple matrix model was parameterized using estimates from our experimental and observational data. This model shows that the parasite-mediated effect on fecundity was sufficient to regulate reindeer densities around observed host densities.
The cumulative effects of climate warming on herbivore vital rates and population dynamics are hard to predict, given that the expected effects differ between seasons. In the Arctic, warmer summers enhance plant growth which should lead to heavier and more fertile individuals in the autumn. Conversely, warm spells in winter with rainfall (rain-on-snow) can cause 'icing', restricting access to forage, resulting in starvation, lower survival and fecundity. As body condition is a 'barometer' of energy demands relative to energy intake, we explored the causes and consequences of variation in body mass of wild female Svalbard reindeer (Rangifer tarandus platyrhynchus) from 1994 to 2015, a period of marked climate warming. Late winter (April) body mass explained 88% of the between-year variation in population growth rate, because it strongly influenced reproductive loss, and hence subsequent fecundity (92%), as well as survival (94%) and recruitment (93%). Autumn (October) body mass affected ovulation rates but did not affect fecundity. April body mass showed no long-term trend (coefficient of variation, CV = 8.8%) and was higher following warm autumn (October) weather, reflecting delays in winter onset, but most strongly, and negatively, related to 'rain-on-snow' events. October body mass (CV = 2.5%) increased over the study due to higher plant productivity in the increasingly warm summers. Density-dependent mass change suggested competition for resources in both winter and summer but was less pronounced in recent years, despite an increasing population size. While continued climate warming is expected to increase the carrying capacity of the high Arctic tundra, it is also likely to cause more frequent icing events. Our analyses suggest that these contrasting effects may cause larger seasonal fluctuations in body mass and vital rates. Overall our findings provide an important 'missing' mechanistic link in the current understanding of the population biology of a keystone species in a rapidly warming Arctic.
Summary 1.It is well known that gastrointestinal nematodes can have a significant impact on the growth of farmed ruminants. The clinical signs of these parasites are often subtle, with production losses mainly due to reductions in host appetite and gut function. However, little is known about the impact of this widespread group of parasites on wild ruminants. We use experiments and cross-sectional data to investigate the effects of gastrointestinal nematodes on a wild host, the Svalbard reindeer. 2. Individually marked reindeer were treated for parasites. Their body mass, back fat depth and fecundity were compared with the control group one year later. The effect of treatment on worm burdens was investigated in a subsample of animals that were culled 3 and 6 months after treatment. Also, the relationship between the intensity of infection and body mass, back fat depth and host pregnancy rates was investigated in crosssectional data from culled reindeer. 3. The anthelmintic treatment caused an increase in the body mass, back fat depth and fecundity of the reindeer. Treatment depressed the abundance of adult parasites of Ostertagia gruehneri for at least 6 months, but had no significant effect on the abundance of adults of the other dominant parasite species, Marshallagi marshalli , or the abundance of larval stages of either species. 4. In the cross-sectional study, the probability of a reindeer being pregnant in late winter was negatively related to the abundance of adult O. gruehneri when controlling for host body mass. However, no clear evidence were found for an effect of parasitism on host condition in the cross-sectional study. 5. Our experimental results show for the first time in a natural ruminant host population that gastrointestinal nematodes can have a significant effect on host condition and fecundity. However, effects of infection on host condition was not detectable in the cross-sectional study. Also, we show that the experimental effects on host condition and fecundity is most likely to be due to a negative effect of O. gruehneri , while the experimental design did not allow detection of potential negative effects of M. marshalli .
Intensities of warble fly larvae, Hypoderma tarandi (L.), were examined in slaughtered reindeer (Rangifer tarandus tarandus L.) from different summer grazing areas of Finnmark County, northern Norway. To test the hypothesis that larval abundance decreases with increase in post-calving migration distance (i.e., distance from calving grounds), herds with differing migration distances were sampled. The prevalence of infection in the total sample of 1168 animals was 99.9%. The study revealed significant differences in larval abundance among herds from different summer grazing areas. Herds with post-calving migrations have significantly lower larval abundances than herds remaining on or near the calving grounds for the whole summer. Between-herds variation in abundance of H. tarandi larvae is assumed to reflect differing densities of the infective stage (adult flies) on the herds' summer ranges. Larval abundance in a herd is in turn negatively correlated with the distance between the main larval shedding areas (i.e., calving grounds) and the areas of greatest transmission (i.e., summer pastures). These results are discussed in relation to transmission of other parasites common to Rangifer and suggest that this host's post-calving migration may be a behavioural adaptation that reduces levels of parasitic infections.
Assessing the role of weather in the dynamics of wildlife populations is a pressing task in the face of rapid environmental change. Rodents and ruminants are abundant herbivore species in most Arctic ecosystems, many of which are experiencing particularly rapid climate change. Their different life-history characteristics, with the exception of their trophic position, suggest that they should show different responses to environmental variation. Here we show that the only mammalian herbivores on the Arctic islands of Svalbard, reindeer (Rangifer tarandus) and sibling voles (Microtus levis), exhibit strong synchrony in population parameters. This synchrony is due to rain-on-snow events that cause ground ice and demonstrates that climate impacts can be similarly integrated and expressed in species with highly contrasting life histories. The finding suggests that responses of wildlife populations to climate variability and change might be more consistent in Polar regions than elsewhere owing to the strength of the climate impact and the simplicity of the ecosystem.
The observation that the total abundance of adult nematodes in the abomasum of Svalbard reindeer increases between October and April suggests adaptation to cope with the Arctic winter. Here we investigate the extent to which selection has led to similar life-history strategies in the 3 most numerous trichostrongyle species. The life-histories are found to differ markedly. We use flexible statistical models for the abundance and dispersion of parasites in the host population. One of the taxa, Marshallagia marshalli, was most abundant and had its highest egg output in the winter. In contrast, the abundance of the most common taxa, Ostertagia gruehneri, m. gruehneri was stable or declined from autumn to late winter, and the closely related taxa, O. gruehneri, m. arcticus, showed a similar over winter drop. The faecal egg output of these 2 taxa was highest in summer, as found in temperate trichostrongyle species. Despite the apparent contamination of summer pastures with O. gruehneri, calves showed negligible burdens until their second summer and the abundance of infection reached an asymptote within their third year. In contrast, the abundance of M. marshalli in calves showed a rapid increase over the first summer and by late winter was similar to peak levels found in adults (8000 worms). This increase could not be accounted for by the developing abomasum larvae population and is therefore evidence for transmission over the winter for this taxa. While M. marshalli showed little between-year variation, O. gruehneri showed 2-fold fluctuation in the abundance of infection. O. gruehneri may therefore play a role in the fluctuating population dynamics of the host. Since there was no apparent decline in abundance with host age in any of the 3 taxa there was no evidence of reindeer mounting an immune response.
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