Behavioural trade‐offs in response to external stimuli: time allocation of an Arctic ungulate during varying intensities of harassment by parasitic flies

Abstract

Summary1. Macroparasites may be a major factor shaping animal behaviour. Tundra ecosystems inhabited by caribou and reindeer (Rangifer tarandus) are known for large concentrations of ectoparasites including mosquitoes (Culicidae) and black flies (Simuliidae), as well as endoparasitic oestrid flies (Oestridae). 2. Increased intensity and duration of insect harassment because of climatic warming is hypothesized as a potential factor in recent declines of Rangifer across the circumpolar north. Although there is a well-observed relationship between insect harassment and caribou ⁄ reindeer behaviour, the influence of ecto-relative to endoparasitic species is unclear. Climatic changes may favour the activity patterns, distribution or abundance of certain insect species; thus, understanding differential effects on the behaviour of Rangifer is important. 3. We recorded caribou behaviour using group scan and focal sampling methods, while simultaneously trapping insects and recording weather conditions on the postcalving ⁄ summer range of the Bathurst barren-ground caribou herd in Northwest Territories and Nunavut, Canada, during 2007-2009. 4. We developed statistical model sets representing hypotheses about the effects of insects, weather, habitat ⁄ location, and date ⁄ time on caribou behaviour. We used multinomial logistic regression models to explore factors affecting the relative dominance of behaviour types within groups of caribou and fractional multinomial logistic regression models to determine factors influencing time allocation by individual caribou. We examined changes in feeding intensity using fractional logistic regression. 5. Relative dominance of insect avoidance behaviour within caribou groups and time allocation to insect avoidance by individual caribou increased when oestrid flies were present or black flies were active at moderate-high levels. Mosquito activity had relatively little effect on caribou behaviour. Time spent feeding was reduced by the greatest degree when all three insect types were present in combination. Feeding intensity was influenced to a greater extent by the accumulation of growing degree days over the course of the postcalving ⁄ summer season than by insect activity. Changes in Arctic systems that increase the activity ⁄ abundance of ecto-and endoparasites could have implications for the productivity of Rangifer populations.

Causes and Consequences of Broad-Scale Changes in the Distribution of Migratory Caribou (<i>Rangifer tarandus</i>) of Southern Hudson Bay

“…This difference may be attributable, in part, to vegetation; coastal habitats typically contain a higher proportion of emerging herbaceous plants compared to areas south of the tree line (Riley, 2011). Furthermore, predation risk and insect harassment can also decrease feeding efficiency in ungulates (Hunter and Skinner, 1998;Barten et al, 2001;Laundré et al, 2001;Hebblewhite et al, 2008), including caribou (Hagemoen and Reimers, 2002;Bergerud et al, 2008;Witter et al, 2012). We surmise that decreased intraspecific competition, relief from biting insects, and lower wolf density on the coast, as reported for other coastal caribou summering areas (Garner and Reynolds, 1986;Heard et al, 1996), may have collectively enhanced the nutritional status of female caribou near the SHB coast.…”

Observed and predicted effects of climate change on Arctic caribou and reindeer

“…However, when Colman et al (2003) tested this idea, they found that reindeer did not increase grazing time in the evening to compensate for reduced grazing on days when insect harassment was greater. Similarly, Witter et al (2012b) found no compensatory grazing by caribou after days when foraging opportunities were lost to insect harassment.…”

“…There are, of course, the direct effects of the parasitic burden that results from successful parasite attacks, with increasing parasite load in an individual associated with decreasing body condition and reproduction (Thomas and Kiliaan 1990;Albon et al 2002;Hughes et al 2009;Ballesteros et al 2012;Cuyler et al 2012;Pachkowski et al 2013). Second, the behavioural response of Rangifer to insect harassment is detrimental to individuals through a reduction in time spent foraging and increased energy expenditure (Downes et al 1986;Ion and Kershaw 1989;Mörschel and Klein 1997;Hagemoen and Reimers 2002;Skarin et al 2010;Witter et al 2012b). These behavioural responses can result in reduced body condition going into the winter (Helle and Tarvainen 1984;Helle and Kojola 1994;Weladji et al 2003), with negative implications for survival and fecundity (Thomas and Kiliaan 1998a).…”

In a warmer Arctic, mosquitoes avoid increased mortality from predators by growing faster

“…In 2012, when the ponds melted earlier, mosquito emergence closely coincided with caribou calving. Insect harassment drives caribou movement [13,39,40], often to insect-free areas such as snow patches and wind-exposed sites at high elevations that offer less food [13,41,42]. Reduced food intake, caused by phenological mismatch with plants or increased time spent avoiding insect harassment, can decrease calf production and increase calf mortality [27].…”