Environmental oestrogens cause predation-induced population decline in a freshwater fish

Abstract

Understanding population-level effects of environmental stressors on aquatic biota requires knowledge of the direct adverse effects of pollutants on individuals and species interactions that relate to survival and reproduction. Here, we connect behavioural assays with survival trials and a modelling approach to quantify changes in antipredator escape performance of a larval freshwater fish following exposure to an environmental oestrogen, and predict changes in population abundance. We quantified the effects of short-term (21 days) exposure to 17β-oestradiol (E2) on the antipredator escape performance of larval fathead minnows (Pimephales promelas) and the probability of predation by a natural predator, the bluegill sunfish (Lepomis macrochirus). Compared with unexposed minnows, minnows exposed to environmentally relevant concentrations of E2 that approach total oestrogenic activity of wastewater-dominated environments (38 and 103 ng l−1) had delayed response times and slower escape speeds, and were more susceptible to predation. Incorporating these data into a stage-structured population model demonstrated that enhanced predation mortality at the larval stage can result in population declines. These results indicate that subtle, sub-lethal shifts in the behaviour of individuals due to human-mediated environmental change can impact species interactions with measurable population-level effects. Such changes have the potential to alter higher-order trophic interactions and disrupt aquatic communities.

Temperature and Estrogen Alter Predator–Prey Interactions between Fish Species

“…Increased predation mortality following exposure to environmental contaminants has been reported in a number of aquatic species ( Weis et al. 2001 ), including P. promelas ; for example, Rearick et al. (2018) showed that the survival of larvae exposed to low or high concentrations of 17β-estradiol was reduced by 10% and 11%, respectively, in predation trials involving sunfish.…”

“…2009 ; Ward et al. 2017 ) suggesting that it has the potential to alter predator–prey dynamics ( Rearick et al. 2018 ); however, whether such changes translate into higher predation rates and how E1 affects predator efficacy is unknown.…”

Environmental estrogen exposure disrupts sensory processing and nociceptive plasticity in the cephalopod, Euprymna scolopes

“…In fish, water-borne estrogenic pollutants have wide-ranging behavioral and physiological effects. Effects include alterations to behaviors that are also affected by nociceptive plasticity, such as aggression, anxiety and responses to predators (Dang et al, 2017;Dzieweczynski et al, 2014;Rearick et al, 2018;Volkova et al, 2015); however, whether similarly complex effects occur in aquatic invertebrates is less clear.…”

“…These effects are likely to extend to invertebrates such as cephalopods, which are important components of inshore food webs as eggs laid in the nearshore benthos, and juvenile and adult stages inhabiting shallow coastal waters. Injured and compromised prey represent preferred targets for many predatory species (Bowerman et al, 2010;Crook et al, 2014;Krumm et al, 2010;Semlitsch, 1990), and there is evidence that predation rates are affected by estrogen exposure in some fish species (Rearick et al, 2018); thus, any disruption to behavioral and neural plasticity processes that underlie adaptive responses to injury may have wide-ranging effects on marine ecosystems.…”

Exploring the Impacts of Methylmercury‐Induced Behavioral Alterations in Larval Yellow Perch in Lake Michigan Using an Individual‐Based Model

“…Similarly, impairments to swimming and foraging behaviors for fry of Lake Trout Salvelinus namaycush suffering from thiamine deficiency led to increased starvation and, when coupled with a high predation rate, resulted in a collapse of a simulated cohort (Ivan et al 2018). Furthermore, larval Fathead Minnows exposed to 17β‐estradiol exhibited reduced antipredator escape performance, and the resulting higher predation mortality rate led to a simulated population decline (Rearick et al 2018). Therefore, it is important that fishery managers consider the sublethal effects of contaminants when assessing wild fish populations.…”