Abstract

Uncertainty in risks posed by emerging stressors such as synthetic hormones impedes conservation efforts for threatened vertebrate populations. Synthetic hormones often induce sex‐biased perturbations in exposed animals by disrupting gonad development and early life‐history stage transitions, potentially diminishing per capita reproductive output of depleted populations and, in turn, being manifest as Allee effects. We use a spatially explicit biophysical model to evaluate how sex‐biased perturbation in life‐history traits of individuals (maternal investment in egg production and male‐skewed sex allocation in offspring) modulates density feedback control of year‐class strength and recovery trajectories of a long‐lived, migratory fish—shovelnose sturgeon (Scaphirhynchus platorynchus)—under spatially and temporally dynamic synthetic androgen exposure and habitat conditions. Simulations show that reduced efficiency of maternal investment in gonad development prolonged maturation time, increased the probability of skipped spawning, and, in turn, shrunk spawner abundance, weakening year‐class strength. However, positive density feedback disappeared (no Allee effect) once the exposure ceased. By contrast, responses to the demographic perturbation manifested as strong positive density feedback; an abrupt shift in year‐class strength and spawner abundance followed after more than two decades owing to persistent negative population growth (a strong Allee effect), reaching an alternative state without any sign of recovery. When combined with the energetic perturbation, positive density feedback of the demographic perturbation was dampened as extended maturation time reduced the frequency of producing male‐biased offspring, allowing the population to maintain positive growth rate (a weak Allee effect) and gradually recover. The emergent patterns in long‐term population projections illustrate that sex‐biased perturbation in life‐history traits can interactively regulate the strength of density feedback in depleted populations such as Scaphirhynchus sturgeon to further diminish reproductive capacity and abundance, posing increasingly greater conservation challenges in chemically altered riverscapes.

Highlights

  • Human activities have uniquely shaped life-history strategies of wild animal populations by imposing unnatural stress for centuries (Crain, Kroeker, & Halpern, 2008; Hendry, Farrugia, & Kinnison, 2008)

  • Because we lack information on a quantitative relationship between synthetic androgen exposure and Scaphirhynchus sturgeon vitellogenin production, we tested the hypothetical scenarios of 15%, 25%, and 35% reduction in daily vitellogenin production (Figure S2) in fish that are located at the Elkhorn River–Platte River confluence, and these reduction rates in vitellogenin production approximately correspond to the responses in fish exposed to environmentally realistic, low-level synthetic androgens (e.g.,

  • We find that lowered vitellogenin production rate prolongs maturation period and incurs skipped spawning, and, in turn, reduces spawner abundance, weakening year-class strength

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Summary

| INTRODUCTION

Human activities have uniquely shaped life-history strategies of wild animal populations by imposing unnatural stress for centuries (Crain, Kroeker, & Halpern, 2008; Hendry, Farrugia, & Kinnison, 2008). Resulting skewed adult sex ratio may manifest as a mate-finding Allee effect (Gascoigne et al, 2009) by impairing reproduction density-dependently (e.g., a decline in mating success), impeding recovery and posing extinction risk for depleted populations as abundance declines further Such human-mediated modification in demographic traits has been reported in exploited populations with sex-biased mortality (Grüebler et al, 2008; Molnar, Derocher, Lewis, & Taylor, 2007). We use a spatially explicit individual-based biophysical model that accounts for sex-specific life-history traits to evaluate how sex-biased perturbation in energetics (reduced maternal investment in egg production) and demographics (male-skewed sex allocation in offspring)—two commonly reported symptoms of synthetic androgens—disrupts density-dependent reproductive processes to control year-class success and population recovery under spatially and temporally dynamic exposure and habitat conditions

| MATERIALS AND METHODS
Basic principles
Emergence
Observation
Findings
| DISCUSSION
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