Municipal wastewaters are a complex mixture containing estrogens and estrogen mimics that are known to affect the reproductive health of wild fishes. Male fishes downstream of some wastewater outfalls produce vitellogenin (VTG) (a protein normally synthesized by females during oocyte maturation) and early-stage eggs in their testes, and this feminization has been attributed to the presence of estrogenic substances such as natural estrogens [estrone or 17-estradiol (E2)], the synthetic estrogen used in birth-control pills [17␣-ethynylestradiol (EE2)], or weaker estrogen mimics such as nonylphenol in the water. Despite widespread evidence that male fishes are being feminized, it is not known whether these low-level, chronic exposures adversely impact the sustainability of wild populations. We conducted a 7-year, wholelake experiment at the Experimental Lakes Area (ELA) in northwestern Ontario, Canada, and showed that chronic exposure of fathead minnow (Pimephales promelas) to low concentrations (5-6 ng⅐L ؊1 ) of the potent 17␣-ethynylestradiol led to feminization of males through the production of vitellogenin mRNA and protein, impacts on gonadal development as evidenced by intersex in males and altered oogenesis in females, and, ultimately, a near extinction of this species from the lake. Our observations demonstrate that the concentrations of estrogens and their mimics observed in freshwaters can impact the sustainability of wild fish populations.endocrine disrupters ͉ fathead minnow ͉ municipal wastewaters ͉ population-level effects ͉ whole-lake experiment
Methylmercury contamination of fisheries from centuries of industrial atmospheric emissions negatively impacts humans and wildlife worldwide. The response of fish methylmercury concentrations to changes in mercury deposition has been difficult to establish because sediments/soils contain large pools of historical contamination, and many factors in addition to deposition affect fish mercury. To test directly the response of fish contamination to changing mercury deposition, we conducted a whole-ecosystem experiment, increasing the mercury load to a lake and its watershed by the addition of enriched stable mercury isotopes. The isotopes allowed us to distinguish between experimentally applied mercury and mercury already present in the ecosystem and to examine bioaccumulation of mercury deposited to different parts of the watershed. Fish methylmercury concentrations responded rapidly to changes in mercury deposition over the first 3 years of study. Essentially all of the increase in fish methylmercury concentrations came from mercury deposited directly to the lake surface. In contrast, <1% of the mercury isotope deposited to the watershed was exported to the lake. Steady state was not reached within 3 years. Lake mercury isotope concentrations were still rising in lake biota, and watershed mercury isotope exports to the lake were increasing slowly. Therefore, we predict that mercury emissions reductions will yield rapid (years) reductions in fish methylmercury concentrations and will yield concomitant reductions in risk. However, a full response will be delayed by the gradual export of mercury stored in watersheds. The rate of response will vary among lakes depending on the relative surface areas of water and watershed.bioaccumulation ͉ mercury methylation ͉ stable isotopes ͉ whole-ecosystem experimentation ͉ methylmercury
There is a pressing need to understand how ecosystems will respond to climate change. To date, no long-term empirical studies have confirmed that fish populations exhibit adaptive foraging behavior in response to temperature variation and the potential implications this has on fitness. Here, we use an unparalleled 11-y acoustic telemetry, stable isotope, and mark-recapture dataset to test if a population of lake trout (Salvelinus namaycush), a coldwater stenotherm, adjusted its use of habitat and energy sources in response to annual variations in lake temperatures during the open-water season and how these changes translated to the growth and condition of individual fish. We found that climate influenced access to littoral regions in spring (data from telemetry), which in turn influenced energy acquisition (data from isotopes), and growth (mark-recapture data). In more stressful years, those with shorter springs and longer summers, lake trout had reduced access to littoral habitat and assimilated less littoral energy, resulting in reduced growth and condition. Annual variation in prey abundance influenced lake trout foraging tactics (i.e., the balance of the number and duration of forays) but not the overall time spent in littoral regions. Lake trout greatly reduced their use of littoral habitat and occupied deep pelagic waters during the summer. Together, our results provide clear evidence that climate-mediated behavior can influence the dominant energy pathways of top predators, with implications ranging from individual fitness to food web stability.food web | climate change | habitat coupling | lake trout | north-temperate lake T here is growing urgency to understand how ecosystems are responding to climate change (1, 2). Recent work, using latitudinal gradients as proxies to warming, has argued that the behavioral responses of mobile top predators to changing temperatures can drive fundamental shifts in aquatic food webs by altering the coupling of major energy pathways (3, 4). Although this work is intriguing, no one has yet examined long-term empirical data that have explicitly tested if populations of top predators can shift their foraging behavior in response to annual changes in temperature or has evaluated what implications this might have for individual fitness. Temporal studies are critically important in this context because they control for the ecosystemspecific adaptations that can confound latitudinal studies and instead focus on the active responses to changing conditions that are highly relevant to understanding the impacts of climate change.Mobile top predators display adaptive foraging behavior by moving across spatially disparate habitats in response to changing conditions, most notably prey densities. For example, birds feed on both terrestrial and aquatic prey, effectively coupling these ecosystems (5). Habitat coupling can also occur within ecosystems and has been well described in freshwater lakes, where predatory fish feed upon prey supported by dissimilar energy sources, such as offsho...
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.
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