Direct and indirect responses of a freshwater food web to a potent synthetic oestrogen

Abstract

Endocrine-disrupting chemicals (EDCs) in municipal effluents directly affect the sexual development and reproductive success of fishes, but indirect effects on invertebrate prey or fish predators through reduced predation or prey availability, respectively, are unknown. At the Experimental Lakes Area in northwestern Ontario, Canada, a long-term, whole-lake experiment was conducted using a before-after-control-impact design to determine both direct and indirect effects of the synthetic oestrogen used in the birth control pill, 17α-ethynyloestradiol (EE2). Algal, microbial, zooplankton and benthic invertebrate communities showed no declines in abundance during three summers of EE2 additions (5–6 ng l −1 ), indicating no direct toxic effects. Recruitment of fathead minnow ( Pimephales promelas ) failed, leading to a near-extirpation of this species both 2 years during (young-of-year, YOY) and 2 years following (adults and YOY) EE2 additions. Body condition of male lake trout ( Salvelinus namaycush ) and male and female white sucker ( Catostomus commersonii ) declined before changes in prey abundance, suggesting direct effects of EE2 on this endpoint. Evidence of indirect effects of EE2 was also observed. Increases in zooplankton, Chaoborus , and emerging insects were observed after 2 or 3 years of EE2 additions, strongly suggesting indirect effects mediated through the reduced abundance of several small-bodied fishes. Biomass of top predator lake trout declined by 23–42% during and after EE2 additions, most probably an indirect effect from the loss of its prey species, the fathead minnow and slimy sculpin ( Cottus cognatus ). Our results demonstrate that small-scale studies focusing solely on direct effects are likely to underestimate the true environmental impacts of oestrogens in municipal wastewaters and provide further evidence of the value of whole-ecosystem experiments for understanding indirect effects of EDCs and other aquatic stressors.

Assessing variation in the potential susceptibility of fish to pharmaceuticals, considering evolutionary differences in their physiology and ecology

“…Some models have indicated that short-lived, asynchronous spawning fish, such as the fathead minnow, may be more susceptible to population decline compared with longer-lived, seasonal spawning brook trout (Salvelinus fontinalis), following simulated multi-generation exposures to endocrine active chemicals [41]. These findings are consistent with studies on an experimental lake dosed for 3 years with the synthetic oestrogen EE2, which resulted in significant population decline in fathead minnows, but not the longer-lived, demersal white sucker (Catostomus commersonii) [15]. There is also some indication of increasing, heritable susceptibility to EE2 over generations, according to mesocosm studies on fathead minnows [42], and this is supported by laboratory life cycle studies on fathead minnows and zebrafish [43,44].…”

“…Other small fish species, such as the Chinese rare minnow (Gobiocypris rarus) may be even more susceptible to EE2 [45]. It is also possible that longer-term exposures to chemicals, including pharmaceuticals, may eventually become more problematic for longer-lived species with relatively low lifetime fecundity and inflexible lifehistory strategies [38,39] and/or fish species occurring higher in the food chain [15].…”

“…scavenging on the carcasses of treated cattle [10,11]. In another case, the contraceptive oestrogen 17a-ethinyloestradiol (EE2) has been linked directly with population-level risks in wild fish, owing to feminization in males and reduced fertility in both sexes of several fish species [12][13][14][15].…”

Avian scavengers and the threat from veterinary pharmaceuticals

“…Studies have highlighted the chronic impacts that certain drugs can have on aquatic organisms, especially fish [1][2][3][4][5][6]. In terrestrial systems, PIE has received less attention, yet one drug has had an acute impact on global population sizes of at least three bird species.…”

Molecular and cellular effects of contamination in aquatic ecosystems

“…Segner 2011, Shore et al 2014). An example is provided by the experimental lake study of Kidd et al (2007Kidd et al ( , 2012: dosing a Canadian lake over 3 years with about 5 ng L −1 of the pharmaceutical ethinylestradiol did not cause any mortalities among the exposed fish species but caused specific molecular, cellular and physiological changes which eventually inhibited successful recruitment thereby leading to extinction of fish species such as fathead minnow. Interestingly, not all fish species were affected, what appears to be on one hand related to differences of physiological properties among the exposed species, but on the other hand, it relates to indirect effects of the chemical exposure on the food web of the lake.…”