Divergent density feedback control of migratory predator recovery following sex-biased perturbations

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.

Keywords: agent‐based modeling; alternative states; early life history; endangered species; endocrine disruptors; spatially explicit models.

Figure 1

Shovelnose sturgeon Scaphirhynchus platorynchus. (a) Adult shovelnose sturgeon; (b) a schematic of the spatially explicit individual‐based biophysical model used in this study

Figure 2

Map of the study system, lower Platte River, Nebraska, USA

Figure 3

Population dynamics and density dependence in population growth of shovelnose sturgeon population. (a) Population projections during exposure and recovery under four synthetic androgen scenarios: a baseline scenario; an energetic perturbation (reduced maternal investment in gonad development) scenario with three exposure levels (shown as biomass relative to the baseline); a demographic perturbation (male‐biased sex allocation in offspring) scenario; and a combined scenario of energetic and demographic perturbations. (b) Relationships between population biomass and per capita population growth rate, ln(N_{t +1}/N_t), during exposure (baseline: y = 0.32x–1.3, r = .26; energetic perturbation: y = 0.24x–1.0, r = .26; demographic perturbation: y = 0.29x–1.2, r = .28; and combined: y = 0.20x–0.84, r = .25) and recovery (baseline: y = 0.49x–2.0, r = .43; energetic perturbation: y = 0.0098x–0.031 r = .023; demographic perturbation: y = 0.083x–0.33, r = .13; and combined: y = 0.072x–0.25, r = .11)

Figure 4

Deviation (%) compared to the baseline scenario in life‐history traits of shovelnose sturgeon populations. (a) Proportion of mature females in the reproductive cycle, recruit number, reproductive female number, and spawner biomass under energetic perturbation scenarios; (b) relationship between relative reproductive female number and spawner biomass or recruit number during exposure and recovery under energetic perturbation scenarios; (c) adult sex ratio, recruit number, reproductive female number, and spawner biomass under demographic perturbation scenarios; and (d) relationship between adult sex ratio and reproductive female number, spawner biomass, or recruit number during exposure and recovery under demographic perturbation scenarios. In (a) and (c), black circles indicate annual mean values of life‐history traits. In (b) and (d), data points show mean values from low, medium, and high androgen exposure levels

Figure 5

Deviation (%) compared to the baseline scenario in life‐history traits of shovelnose sturgeon populations under combined scenario of energetic and demographic perturbations. (a) adult sex ratio, proportion of adult females in the reproductive cycle, recruit number, reproductive female number, and spawner biomass; (b) relationship between relative reproductive female number and spawner biomass or recruit number during exposure and recovery; and (c) relationship between adult sex ratio and reproductive female number, spawner biomass, or recruit number during exposure and recovery. In a, black circles indicate annual mean values of life‐history traits. In (b) and (c), data points show mean values from low, medium, and high androgen exposure levels