Abiotic and Biotic Factors Associated with Tick Population Dynamics on a Mammalian Host: Ixodes hexagonus Infesting Otters, Lutra lutra

Lutra lutra. PLoS ONE 7(10): e47131. doi:10.1371/journal.pone.0047131 Abiotic and Biotic Factors Associated with Tick Population Dynamics on a Mammalian Host: Ixodes hexagonus Infesting Otters, Lutra lutra Ellie Sherrard-Smith 0 Elizabeth Chadwick 0 Joanne Cable 0 Roman Ganta, Kansas State University, United States of America 0 Organisms and the Environment, Cardiff University , Cardiff , United Kingdom The Eurasian otter, Lutra lutra, hosts several parasites with zoonotic potential. As this semiaquatic mammal has large ranges across terrestrial, freshwater and marine habitats, it has the capacity for wide dispersion of pathogens. Despite this, parasites of otters have received relatively little attention. Here, we examine their ectoparasite load and assess whether this is influenced by abiotic or biotic variables. Climatic phenomena such as the North Atlantic Oscillation (NAO) affect weather conditions in northern Europe. Consequently parasite distributions, particularly species with life stages exposed to the external environment, can be affected. We assessed the extent to which inter-annual variations in large-scale weather patterns (specifically the NAO and Central England (CE) temperatures) and host characteristics influenced tick prevalence and intensity. Ectoparasites consisted of a single species, the nidiculous tick Ixodes hexagonus (prevalence = 24.3%; mean intensity = 7.2; range = 1-122; on n = 820 otter hosts). The prevalence, but not intensity of infestation, was associated with high CE temperatures, while both prevalence and intensity were associated with positive phases of the NAO. Such associations indicate that I. hexagonus are most abundant when weather conditions are warmer and wetter. Ticks were more prevalent on juvenile than sub-adult or adult otters, which probably reflects the length of time the hosts spend in the holt where these ticks quest. High tick number was associated with poor host condition, so either poor condition hosts are more susceptible to ticks, or tick infestations negatively impact on host condition. Otters are clearly an important and common host for I. hexagonus, which has implications for vector-borne diseases. This work is the first to consider the impacts of long-term weather patterns on I. hexagonus and uses wild-animal cadavers to illustrate the importance of abiotic and biotic pressures impacting parasitic populations. - Funding: Ellie Sherrard-Smith was supported by a Natural Environment Research Council Studentship (NERC),(NER/0329013) with Case Partner, James Williams and the Somerset Otter Group. Joanne Cable was funded by an Advanced NERC Fellowship (NER/J/S/2002/00706). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. Current change in climate (the long-term average meteorological conditions of a region [1]) is associated with increases in temperature and precipitation, especially in Northern temperate zones [1]. This influences parasite distributions both directly [2,3] and indirectly, for example via impacts on host range [4,5]. Weather (short-term variation in meteorological conditions) can cause variations in parasite distributions whilst synchronously influencing host abundance [6] but will affect specific host-parasite interactions differently [4,79]. Weather patterns are influenced by climatic phenomena such as the North Atlantic Oscillation (NAO). The NAO affects European climate such that, when in positive phases, northern Europe experiences warmer and wetter conditions [10,11]. Identifying associations between climate and the distribution of vectors over time (e.g. [12,13]) is an essential pre-requisite to understanding public and wildlife health risks resulting from vector-borne infection. Ixodid ticks are vectors for a range of pathogens causing diseases including Lyme disease, Boutonneuse fever, Q fever, tick-borne fever and tick-borne encephalitis [14]. Ixodes hexagonus is an efficient vector of Borrelia burgdorferi, the causative agent of Lyme disease [15] but in the UK, I. ricinus has received most attention because of its ubiquitous nature and association with transmission of pathogens to humans and livestock [14]. The distribution of I. ricinus is influenced by weather [16,17] and the presence of suitable hosts and habitat [18]. Temperature increases are associated with increasing population density and geographic range of I. ricinus, a European tick [17,19], and other tick species such as the North American species I. scapularis. [20]. The majority of ixodid ticks require .80% relative humidity for survival off the host [2123] and as such, positive phases of the NAO may benefit ixodid ticks by creating suitably humid weather. Landscape, habitat use and local weather conditions have been associated with tick distributions previously [16,17,19,20,24,25]. The impact of such environmental variables on host-parasite interactions is, however, highly variable [26]. Mustelids have been associated with the nidiculous (burrow or nest dwelling) tick I. hexagonus [24] but the relationship between I. hexagonus and weather conditions has not been examined previously. The Eurasian otter, Lutra lutra, is a top predator in the UK and a sentinel of freshwater health [27]. Otters are wide ranging opportunistic predators that feed in terrestrial, freshwater and marine habitats [28]. They are therefore potentially exposed to a wide diversity of pathogens and a great deal can be learned about the distribution of parasites in UK ecosystems by screening such a generalist host. Here, we identified the tick species that use otters as a host. Next, we investigated how weather patterns and host characteristics are associated with tick infestations of otters in England and Wales. Specifically, we hypothesised that tick occurrence (prevalence and intensity) would be positively correlated with temporal variation in: i) the NAO (associated with warmer and wetter weather in the UK), and; ii) higher Central England (CE) temperatures (a long-term record of temperature in central England, see Materials and Methods). Based on these findings we hypothesised that spatial variation in tick counts among meteorologically distinct regions of the UK would correlate positively with rainfall and temperature. Tick species Tick (Ixodes hexagonus) prevalence on Eurasian otters, between 2004 and 2010, was 24.3% (199 out of 820) (Figure 1). On some hosts, all post-hatch tick life stages (larva, nymph and adults) were recovered (18 cases), but almost 40% of hosts had only one life stage present at collection (Larvae = 13 cases, Nymph = 40 cases, Adult = 26 cases) (Table 1). Infested otters were widespread across England and Wales (Figure 1) with no evidence of clustering of infestation within the otter distribution (Ripleys K analysis at the 95% confidence level using radii rangi (...truncated)