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1. Prey responses to high predation risk can be morphological or behavioural and ultimately come at the cost of survival, growth, body condition, or reproduction. These sub-lethal predator effects have been shown to be mediated by physiological stress. We tested the hypothesis that elevated glucocorticoid concentrations directly cause a decline in reproduction in individual free-ranging female snowshoe hares, Lepus americanus. We measured the cortisol concentration from each dam (using a faecal analysis enzyme immunoassay) and her reproductive output (litter size, offspring birth mass, offspring right hind foot (RHF) length) 30 h after birth.
2. In a natural monitoring study, we monitored hares during the first and second litter from the population peak (2006) to the second year of the decline (2008). We found that faecal cortisol metabolite (FCM) concentration in dams decreased 52% from the first to the second litter. From the first to the second litter, litter size increased 122%, offspring body mass increased 130%, and offspring RHF length increased 112%. Dam FCM concentrations were inversely related to litter size (r2 = 0·19), to offspring birth mass (r2 = 0·32), and to offspring RHF length (r2 = 0·64).
3. In an experimental manipulation, we assigned wild-caught, pregnant hares to a control and a stressed group and held them in pens. Hares in the stressed group were exposed to a dog 1–2 min every other day before parturition to simulate high predation risk. At parturition, unsuccessful-stressed dams (those that failed to give birth to live young) and stressed dams had 837% and 214%, respectively, higher FCM concentrations than control dams. Of those females that gave birth, litter size was similar between control and stressed dams. However, offspring from stressed dams were 37% lighter and 16% smaller than offspring from control dams. Increasing FCM concentration in dams caused the decline of offspring body mass (r2 = 0·57) and RHF (r2 = 0·52).
4. This is the first study in a free-ranging population of mammals to show that elevated, predator-induced, glucocorticoid concentrations in individual dams caused a decline in their reproductive output measured both by number and quality of offspring. Thus, we provide evidence that any stressor, not just predation, which increases glucocorticoid concentrations will result in a decrease in reproductive output.
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- Materials and methods
Predation is a central organizing agent shaping population and community processes (Krebs et al. 2001a; Schmitz 2008). Traditionally, ecologists have focused on the direct effects of predation – the killing of prey (Paine 1966; Taylor 1984; Krebs et al. 1995). However, predators also have significant indirect effects on prey populations (see reviews by Lima 1998; Creel & Christianson 2008) and these effects can be as great as their direct effects (Schmitz, Beckerman & O’Brien 1997; Nelson, Matthews & Rosenheim 2004; Preisser, Bolnick & Benard 2005; Pangle, Peacor & Johannsson 2007). Prey responses to the high risk of predation can be morphological such as changes in secondary sexual characteristics and anti-predator defences (Tollrian & Harvell 1999; Day & Young 2004; Vamosi & Schluter 2004) or behavioural such as changes in preferred habitats, in vigilance, and in foraging (Hik 1995; Lima & Bednekoff 1999; Childress & Lung 2003; Armitage 2004; Creel et al. 2005; Winnie & Creel 2007). These responses ultimately come at the cost of survival, growth, body condition, or reproduction (Hik 1995; Boonstra et al. 1998; Krebs et al. 2001a; Olaf & Halle 2004; Bian, Wu & Liu 2005; Hodges, Stefan & Gillis 1999).
The indirect effects of predators act through physiological processes. One of the most conserved processes in vertebrates is the ‘stress response’, defined here as the set of neural and endocrine responses that help restore homeostasis (Sapolsky 1987). Central to the stress response is the activation of the hypothalamic-pituitary-adrenal (HPA) axis and subsequent secretion of glucocorticoids (GC), lasting several minutes to hours (Sapolsky 1992; Wingfield & Romero 2001). A stressor may be any environmental perturbation that disrupts homeostasis, such as harsh weather, habitat changes, anthropogenic disturbances, decreased food availability, and predation attempts (Sapolsky 1987). The presence of short-term elevated GC concentrations facilitates escape from life-threatening situations (Wingfield et al. 1998). However, chronic activation of the HPA axis may trade off future reproduction for present survival (Boonstra & Singleton 1993; Boonstra et al. 1998; Sapolsky, Romero & Munck 2000; Romero & Wikelski 2001; Wingfield & Romero 2001).
Snowshoe hares (Lepus americanus) are an ideal species to study the effects of GCs on reproduction. Snowshoe hares undergo a regular cyclic fluctuation, with 8–10 years between peak densities (Keith 1963; Krebs et al. 1986). As hare populations increase, so do that of their predators, but with a lag of 1–2 years. During the hare population decline, predators are the direct cause of up to 83% of hare deaths (Boutin et al. 1986; Krebs et al. 1995). Hare reproduction also cycles, with maximum rates occurring during the early increase phase (when predator numbers are lowest), but then progressively declining to a nadir during the decline (when predator numbers are at their peak), (Cary & Keith 1979; O'Donoghue & Krebs 1992; O'Donoghue et al. 1997; Stefan & Krebs 2001). Predators could be the indirect cause of this decline, with the inhibition of the gonadal axis being mediated by the stress of high predation risk through the activation of the HPA axis. Boonstra et al. (1998) showed that plasma cortisol concentrations (the major GC in snowshoe hares) fluctuated with the risk of predation, such that hares experiencing a greater risk of predation had higher plasma cortisol. They proposed that chronic stress, as measured by elevated cortisol concentrations, caused the marked deterioration of reproduction during the decline phase.
Here we test the hypothesis that elevated GC concentrations cause a decline in reproduction in free-ranging hares in two ways. First, in a natural monitoring study, we measured cortisol concentrations and reproduction 30 h after birth in natural populations of free-ranging snowshoe hares from 2006 to 2008. We estimated both the hare and the predator density during this time to determine when the population peak and the maximum risk of predation would occur. Second, in an experimental manipulation, we increased the risk of predation during the last two-thirds of gestation in a sample of wild-caught snowshoe hares held in pens and measured cortisol concentrations and reproduction 30 h after birth. Cortisol concentrations were measured non-invasively using a faecal analysis enzyme immunoassay (EIA). Reproduction was measured as litter size, offspring birth mass and RHF length.
In the natural monitoring study, we predicted that as the risk of predation increased faecal cortisol metabolite (FCM) concentrations in dams would increase. In the experimental manipulation, we predicted that FCM concentrations would be higher in the stressed group compared with the control group. In both studies, we expected that an increase in FCM concentration in dams would cause a decrease in their litter size, offspring birth mass and offspring RHF length.