Predator‐induced maternal stress and population demography in snowshoe hares: the more severe the risk, the longer the generational effect

Abstract

The risk of predation can cause strong antipredator behaviors and marked stressinduced changes in physiology. In mothers, predator-induced stress can reduce reproductive fitness and alter offspring phenotypes. Acting via these generational, maternal stress effects, predation risk may continue to influence the demography of prey populations even when the predators are no longer present. The 10-year snowshoe hare cycle is the classic top-down predator-driven example in nature and is caused both by direct mortality and by indirect risk effects. During the decline phase, virtually, all hares die because they are killed and simultaneously hares exhibit pronounced stress effects caused by high predation risk. However, the rapidity of the decline phase varies among cycles. When the decline is extremely rapid, we expect that the risk experienced by hares is much greater than when the decline is prolonged. The enigma of these cycles is the low phase following the decline, when there is little or no population growth in spite of the absence of predators and ample food. Previously, we have shown that predator-induced maternal stress decreases reproduction and compromises the offspring stress axis. Here, we examine how the severity of predation risk during six separate population declines is related to the length of the subsequent low phase. We show that the more severe the decline, as indicated by the greater rate of loss of hares, the longer the subsequent low phase. These results support the hypothesis that the greater the degree of risk, the longer the generational impact on population demography (the longer the low phase of the hare population). Our findings have broad applicability to conservation and management efforts; even when a stressor (predator, human disturbance) is removed or when exposure may be short term (drought, fire or translocation), the signature of the stressor may be evident over several future generations.

Population cycles: generalities, exceptions and remaining mysteries

“…The decline was slower and the trough less deep following the lower but more prolonged peak in 1995-1997 compared to that of 2012 from which the population had still not recovered five years later. Snowshoe hares show a similar pattern in which more severe declines were associated with longer trough periods (figure 1) [46]. High peaks should be followed by more rapid declines if stress influences the intrinsic condition of the animals.…”

“…This points to the need to know what triggers changes in reproduction associated with outbreak density. As suggested for snowshoe hares, epigenetic changes to genes related to stress responses [46,94] or for grouse [95] and insects [96] to disease resistance, might be occurring.…”

“…This impact is carried over to subsequent generations perhaps through epigenetic changes in expression of stress regulatory genes [3]. For snowshoe hares, the length of the decline phase is related to the rate of population decline suggesting that high levels of predator risk associated with rapid population declines might cause stronger and longer lasting epigenetic influences [46].…”

Demographic drivers of a refugee species: large‐scale experiments guide strategies for reintroductions of hirola

“…Although the reduction in adult survival and calf survival show a clear signature of direct killing by predators, it is conceivable that reductions in pregnancy and parturition could have arisen from carnivoreinduced stress (e.g., Creel et al 2009, Sheriff et al 2015 or behavioral shifts to lower-quality habitats (e.g., Ford et al 2014, Ford and Goheen 2015, Ng'weno et al 2017, although the existence and strength of such effects are idiosyncratic and system specific (Kauffman et al 2010, Middleton et al 2013. First, we conducted our work over a relatively short period of time (3 yr) relative to the lifespan of hirola, during which environmental stochasticity (droughts, floods) was minimal and therefore did not feature in our demographic matrices.…”

Prenatal predatory stress in a wild species of subterranean rodent: Do ecological stressors always have a negative effect on the offspring?

“…In addition to these changes at the individual level, in several species, offspring are influenced by the environmental conditions experienced by their mother, who can affect their progeny not only during gestation but also after birth by altering the quality and quantity of parental care (Bauer et al, ; Mashoodh, Sinal, & Perrot‐Sinal, ; Sheriff, McMahon, Krebs, & Boonstra, ). Focusing on prenatal exposure to predator odors, it has been known that maternal exposure to such odors during pregnancy increases plasma levels of GCs in the mother which in turn may have strong effects on fetal development, litter size, body weight development, and time of sexual maturation of offspring (Apfelbach et al, ; Love, McGowan, & Sheriff, ; Monclús, Tiulim, & Blumstein, ; Vasilieva Parfenova, & Apfelbach, ; Weinstock, ).…”