The ghosts of predators past: Population cycles and the role of maternal programming under fluctuating predation risk

Michael Sheriff, Charles Krebs, Rudy Boonstra

Research output: Contribution to journalArticle

118 Citations (Scopus)

Abstract

Maternal effects may be a major factor influencing the demography of populations. In mammals the transmission of stress hormones between mother and offspring may play an important role in these effects. Laboratory studies have shown that stressors during pregnancy and lactation result in lifelong programming of the offspring phenotype. However, the relevance of these studies to free-living mammals is unclear. The 10-year snowshoe hare (Lepus americanus) cycle is intimately linked to fluctuating predation pressure and predation risk. The enigma of these cycles is the lack of population growth following the decline phase, when the predators have virtually all disappeared and the food supply is ample. We have shown that a predator-induced increase in maternal stress hormone levels resulted in a decline in reproduction. Here we examine population and hormone changes over a four-year period from the increase (2005) to the decline (2008). We report (1) that an index of maternal stress (fecal corticosteroid metabolite [FCM] concentrations) fluctuates in synchrony with predator density during the breeding season; (2) that maternal FCM levels are echoed in their offspring, and this occurs at a population-wide level; and (3) that higher maternal FCM levels at birth are correlated with an increased responsiveness of the hypothalamic-pituitary-adrenal (HPA) axis in their progeny. Our results show an intergenerational inheritance of stress hormones in a free-ranging population of mammals. We propose that the lack of recovery of reproductive rates during the early low phase of the hare cycle may be the result of the impacts of intergenerational, maternally inherited stress hormones caused by high predation risk during the decline phase. © 2010 by the Ecological Society of America.
Original languageEnglish
Pages (from-to)2983-2994
Number of pages12
JournalEcology
Volume91
Issue number10
DOIs
Publication statusPublished - 2010
Externally publishedYes

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population cycle
predation risk
hormone
hormones
predator
predation
predators
adrenal cortex hormones
Lepus americanus
metabolite
mammal
mammals
metabolites
maternal effect
lactation
synchrony
hares
food supply
demography
pregnancy

Cite this

Sheriff, Michael ; Krebs, Charles ; Boonstra, Rudy. / The ghosts of predators past: Population cycles and the role of maternal programming under fluctuating predation risk. In: Ecology. 2010 ; Vol. 91, No. 10. pp. 2983-2994.
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The ghosts of predators past: Population cycles and the role of maternal programming under fluctuating predation risk. / Sheriff, Michael; Krebs, Charles; Boonstra, Rudy.

In: Ecology, Vol. 91, No. 10, 2010, p. 2983-2994.

Research output: Contribution to journalArticle

TY - JOUR

T1 - The ghosts of predators past: Population cycles and the role of maternal programming under fluctuating predation risk

AU - Sheriff, Michael

AU - Krebs, Charles

AU - Boonstra, Rudy

PY - 2010

Y1 - 2010

N2 - Maternal effects may be a major factor influencing the demography of populations. In mammals the transmission of stress hormones between mother and offspring may play an important role in these effects. Laboratory studies have shown that stressors during pregnancy and lactation result in lifelong programming of the offspring phenotype. However, the relevance of these studies to free-living mammals is unclear. The 10-year snowshoe hare (Lepus americanus) cycle is intimately linked to fluctuating predation pressure and predation risk. The enigma of these cycles is the lack of population growth following the decline phase, when the predators have virtually all disappeared and the food supply is ample. We have shown that a predator-induced increase in maternal stress hormone levels resulted in a decline in reproduction. Here we examine population and hormone changes over a four-year period from the increase (2005) to the decline (2008). We report (1) that an index of maternal stress (fecal corticosteroid metabolite [FCM] concentrations) fluctuates in synchrony with predator density during the breeding season; (2) that maternal FCM levels are echoed in their offspring, and this occurs at a population-wide level; and (3) that higher maternal FCM levels at birth are correlated with an increased responsiveness of the hypothalamic-pituitary-adrenal (HPA) axis in their progeny. Our results show an intergenerational inheritance of stress hormones in a free-ranging population of mammals. We propose that the lack of recovery of reproductive rates during the early low phase of the hare cycle may be the result of the impacts of intergenerational, maternally inherited stress hormones caused by high predation risk during the decline phase. © 2010 by the Ecological Society of America.

AB - Maternal effects may be a major factor influencing the demography of populations. In mammals the transmission of stress hormones between mother and offspring may play an important role in these effects. Laboratory studies have shown that stressors during pregnancy and lactation result in lifelong programming of the offspring phenotype. However, the relevance of these studies to free-living mammals is unclear. The 10-year snowshoe hare (Lepus americanus) cycle is intimately linked to fluctuating predation pressure and predation risk. The enigma of these cycles is the lack of population growth following the decline phase, when the predators have virtually all disappeared and the food supply is ample. We have shown that a predator-induced increase in maternal stress hormone levels resulted in a decline in reproduction. Here we examine population and hormone changes over a four-year period from the increase (2005) to the decline (2008). We report (1) that an index of maternal stress (fecal corticosteroid metabolite [FCM] concentrations) fluctuates in synchrony with predator density during the breeding season; (2) that maternal FCM levels are echoed in their offspring, and this occurs at a population-wide level; and (3) that higher maternal FCM levels at birth are correlated with an increased responsiveness of the hypothalamic-pituitary-adrenal (HPA) axis in their progeny. Our results show an intergenerational inheritance of stress hormones in a free-ranging population of mammals. We propose that the lack of recovery of reproductive rates during the early low phase of the hare cycle may be the result of the impacts of intergenerational, maternally inherited stress hormones caused by high predation risk during the decline phase. © 2010 by the Ecological Society of America.

KW - Free-ranging mammal

KW - Lepus americanus

KW - Low phase

KW - Lynx canadensis

KW - Maternal effects

KW - Maternal programming

KW - Nongenetic phenotypic effects

KW - Predation risk

KW - Snowshoe hare

KW - Stress

KW - Ten-year cycle

KW - Yukon Canada.

U2 - 10.1890/09-1108.1

DO - 10.1890/09-1108.1

M3 - Article

VL - 91

SP - 2983

EP - 2994

JO - Ecology

JF - Ecology

SN - 0012-9658

IS - 10

ER -