Abiotic and biotic factors associated with tick population dynamics on a mammalian host: Ixodes hexagonus infesting otters, Lutra lutra

Abstract

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.

Figure 1. Tick distributions across the UK.

Distribution of Ixodes hexagonus infested (dark circles) and uninfested (clear circles) otters in England and Wales. Meteorologically distinct regions (East and Northeast England, East Anglia, Southeast England and Central South, Northwest England and North Wales, South Wales and Southwest England, and Midlands) defined by the Meteorological Office UK Climate Impacts Programme (data available online).

Figure 2. Abiotic impact on tick prevalence.

Probability plot for a model of the association between tick prevalence and the explanatory variables A) Central England Temperature for the 12 month period preceding host death, B) North Atlantic Oscillation for the 12 month period preceding death for each host age class: Dotted line  =  juvenile hosts; Solid line  =  Adult hosts; Dashed line  =  Sub-adult hosts.

Figure 3. The North Atlantic Oscillation impacts tick counts on otters.

Relationship of tick count to mean North Atlantic Oscillation at month of host death. Standard error bars shown.

Figure 4. Abiotic impact on tick intensity.

Mean tick intensity (grey bars) in each meteorologically distinct region (East and Northeast England, East Anglia, Southeast England and Central South, Northwest England and North Wales, South Wales and Southwest England, and Midlands) and corresponding 30 year average (1971–2000) summed mean rainfall (mm) (upper Y-axis), maximum (triangle) and minimum (cross) 30 year (1971–2000) average temperature (°C) for each region (lower Y-axis). Standard error marks for rainfall, maximum and minimum temperature correspond to variability in monthly averages.

Figure 5. Biotic impact on tick count.

Relationship of tick intensity to host condition (K). Standard error bars shown.