ABSTRACT
Animal behaviour is remarkably sensitive to disruption by chemical pollution, with widespread implications for ecological and evolutionary processes in contaminated wildlife populations. ...However, conventional approaches applied to study the impacts of chemical pollutants on wildlife behaviour seldom address the complexity of natural environments in which contamination occurs. The aim of this review is to guide the rapidly developing field of behavioural ecotoxicology towards increased environmental realism, ecological complexity, and mechanistic understanding. We identify research areas in ecology that to date have been largely overlooked within behavioural ecotoxicology but which promise to yield valuable insights, including within‐ and among‐individual variation, social networks and collective behaviour, and multi‐stressor interactions. Further, we feature methodological and technological innovations that enable the collection of data on pollutant‐induced behavioural changes at an unprecedented resolution and scale in the laboratory and the field. In an era of rapid environmental change, there is an urgent need to advance our understanding of the real‐world impacts of chemical pollution on wildlife behaviour. This review therefore provides a roadmap of the major outstanding questions in behavioural ecotoxicology and highlights the need for increased cross‐talk with other disciplines in order to find the answers.
Environmental contamination by pharmaceuticals is global, substantially altering crucial behaviours in animals and impacting on their reproduction and survival. A key question is whether the ...consequences of these pollutants extend beyond mean behavioural changes, restraining differences in behaviour between individuals. In a controlled, two-year, multigenerational experiment with independent mesocosm populations, we exposed guppies (
) to environmentally realistic levels of the ubiquitous pollutant fluoxetine (Prozac). Fish (unexposed:
= 59, low fluoxetine:
= 57, high fluoxetine:
= 58) were repeatedly assayed on four separate occasions for activity and risk-taking behaviour. Fluoxetine homogenized individuals' activity, with individual variation in populations exposed to even low concentrations falling to less than half that in unexposed populations. To understand the proximate mechanism underlying these changes, we tested the relative contribution of variation within and between individuals to the overall decline in individual variation. We found strong evidence that fluoxetine erodes variation in activity between but not within individuals, revealing the hidden consequences of a ubiquitous contaminant on phenotypic variation in fish-likely to impair adaptive potential to environmental change.
One Health Bertram, Michael G.; Costi, Maria Paola; Thoré, Eli S.J. ...
Current biology,
06/2024, Letnik:
34, Številka:
11
Journal Article
Recenzirano
Bertram and colleagues introduce the One Health concept, an interdisciplinary framework that aims to sustainably advance and safeguard the health of humans, animals, and the environment.
Anthropogenic noise is a global pollutant but its potential impacts on early life-stages in fishes are largely unknown. Here, using controlled laboratory experiments, we tested for impacts of ...continuous or intermittent exposure to low-frequency broadband noise on early life-stages of the common goby (Pomatoschistus microps), a marine fish with exclusive paternal care. Neither continuous nor intermittent noise exposure had an effect on filial cannibalism, showing that males were capable and willing to care for their broods. However, broods reared in continuous noise covered a smaller area and contained fewer eggs than control broods. Moreover, although developmental rate was the same in all treatments, larvae reared by males in continuous noise had, on average, a smaller yolk sac at hatching than those reared in the intermittent noise and control treatments, while larvae body length did not differ. Thus, it appears that the increased consumption of the yolk sac reserve was not utilised for increased growth. This suggests that exposure to noise in early life-stages affects fitness-related traits of surviving offspring, given the crucial importance of the yolk sac reserve during the early life of pelagic larvae. More broadly, our findings highlight the wide-ranging impacts of anthropogenic noise on aquatic wildlife living in an increasingly noisy world.
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•Noise exposure during early life-stages affects fitness-related traits in fish.•Noise exposure decreases the yolk sac reserve during early life of pelagic larvae.•Brood size, brood area, and egg density decreased with increased noise.•Noise pollution had a negative effect on egg and larval development.•Highlights the wide-ranging impacts of anthropogenic noise on aquatic wildlife
Natural environments are subject to a range of anthropogenic stressors, with pharmaceutical pollution being among the fastest-growing agents of global change. However, despite wild animals living in ...complex multi-stressor environments, interactions between pharmaceutical exposure and other stressors remain poorly understood. Accordingly, we investigated effects of long-term exposure to the pervasive pharmaceutical contaminant fluoxetine (Prozac) and acute temperature stress on reproductive behaviors and activity levels in the guppy (Poecilia reticulata). Fish were exposed to environmentally realistic fluoxetine concentrations (measured average: 38 or 312 ng/L) or a solvent control for 15 months using a mesocosm system. Additionally, fish were subjected to one of three acute (24 h) temperature treatments: cold stress (18 °C), heat stress (32 °C), or a control (24 °C). We found no evidence for interactive effects of fluoxetine exposure and temperature stress on guppy behavior. However, both stressors had independent impacts. Fluoxetine exposure resulted in increased male coercive copulatory behavior, while fish activity levels were unaffected. Under cold-temperature stress, both sexes were less active and males exhibited less frequent reproductive behaviors. Our results demonstrate that long-term exposure to a common pharmaceutical pollutant and acute temperature stress alter fundamental fitness-related behaviors in fish, potentially shifting population dynamics in contaminated ecosystems.
Micropollutants Bertram, Michael G.; Martin, Jake M.; Wong, Bob B.M. ...
Current biology,
01/2022, Letnik:
32, Številka:
1
Journal Article
Recenzirano
Odprti dostop
In this Quick guide, Bertram et al. highlight the growing problem of micropollutants — a wide array of natural and synthetic organic compounds found in the environment.
Pharmaceutical pollutants constitute a major threat to wildlife because of their capacity to induce biological effects at low doses. One such pollutant is the antidepressant fluoxetine, which has ...been detected in surface waters globally at levels that recent studies suggest can alter physiology and behaviour in aquatic organisms. However, wildlife exposed to pharmaceutical contaminants are typically confronted with multiple stressors simultaneously, including predation risk, which is a particularly important natural stressor that can have direct (e.g. mortality) and indirect (e.g. changed prey behaviour) fitness effects. Accordingly, we investigated potential impacts of environmentally realistic fluoxetine exposure on reproductive behaviour in the guppy (Poecilia reticulata) under predation risk. Specifically, we tested whether fluoxetine exposure altered mating behaviour in male and female guppies in the presence of either a predatory spangled perch (Leiopotherapon unicolor) or a non-predatory rainbowfish (Melanotaenia splendida) control. We found that fluoxetine and the presence of a predatory spangled perch did not interact to affect reproductive behaviour. We also found that, independent of a predatory threat, fluoxetine exposure altered male mating strategy, with males in the high treatment conducting significantly more coercive ‘sneak’ copulations, whereas the number of courtship displays performed was not significantly affected. Moreover, while fluoxetine exposure did not significantly affect the amount of time that males and females spent following one another, we found that females, but not males, followed a potential partner less when in the presence of the predatory fish. Finally, both sexes reacted to the risk of predation by spending less time in close proximity to a predator than a non-predator. In combination, our findings highlight the capacity of fluoxetine to influence processes of sexual selection at field-realistic concentrations and emphasise the importance of considering multiple stressors when assessing impacts of pharmaceutical pollutants on the behaviour of wildlife.
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•Pharmaceutical pollution represents a major global threat to wildlife and ecosystems.•Guppies (P. reticulata) were exposed to fluoxetine at two field-realistic levels.•Male and female guppy reproductive behaviour was assessed under predation risk.•High fluoxetine (350 ng/L) increased male coercive mating behaviour, independent of a predatory threat.•Highlights importance of considering interactions between natural stressors and pharmaceutical pollutants.
Pharmaceutical pollution is now recognised as a major emerging agent of global change. Increasingly, pharmaceutical pollutants are documented to disrupt ecologically important physiological and ...behavioural traits in exposed wildlife. However, little is known about potential impacts of pharmaceutical exposure on among-individual variation in these traits, despite phenotypic diversity being critical for population resilience to environmental change. Furthermore, although wildlife commonly experience multiple stressors contemporaneously, potential interactive effects between pharmaceuticals and biological stressors—such as predation threat—remain poorly understood. To redress this, we investigated the impacts of long-term exposure to the pervasive pharmaceutical pollutant fluoxetine (Prozac®) on among-individual variation in metabolic and behavioural traits, and the combined impacts of fluoxetine exposure and predation threat on mean metabolic and behavioural traits in a freshwater fish, the guppy (Poecilia reticulata). Using a mesocosm system, guppy populations were exposed for 15 months to one of two field-realistic levels of fluoxetine (nominal concentrations: 30 and 300 ng/L) or a solvent control. Fish from these populations were then tested for metabolic rate (oxygen uptake) and behaviour (activity), both before and after experiencing one of three levels of a predation treatment: an empty tank, a non-predatory fish (Melanotaenia splendida) or a predatory fish (Leiopotherapon unicolor). Guppies from both fluoxetine treatments had ∼70% lower among-individual variation in their activity levels, compared to unexposed fish. Similarly, fluoxetine exposure at the higher dosage was associated with a significant (26%) reduction in individual-level variation in oxygen uptake relative to unexposed fish. In addition, mean baseline metabolic rate was disrupted in low-fluoxetine exposed fish, although mean metabolic and behavioural responses to predation threat were not affected. Overall, our study demonstrates that long-term exposure to a pervasive pharmaceutical pollutant alters ecologically relevant traits in fish and erodes among-individual variability, which may be detrimental to the stability of contaminated populations globally.
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•We exposed female guppies (P. reticulata) to fluoxetine and acute predation threat.•Fluoxetine reduced among-individual variation in both metabolic rate and activity.•Fluoxetine caused a non-monotonic reduction in baseline metabolic rate.•Fluoxetine did not affect metabolic and behavioural responses to predation threat.
Pulsatile insulin secretion into the portal vein from the many pancreatic islets of Langerhans is critical for efficient glucose homeostasis. The islets are themselves endogenous oscillators, but ...since they are not physically coupled it is not obvious how their oscillations are synchronized across the pancreas. It has been proposed that synchronization of islets is achieved through periodic activity of intrapancreatic ganglia, and indeed there are data supporting this proposal. Postganglionic nerves are cholinergic, and their product, acetylcholine, can influence islet β-cells through actions on M3 muscarinic receptors which are coupled to Gq type G-proteins. In addition, the neurons secrete several peptide hormones that act on β-cell receptors. The data supporting synchronization via intrapancreatic ganglia are, however, limited. In particular, it has not been shown that trains of muscarinic pulses are effective at synchronizing islets in vitro. Also, if as has been suggested, there is a ganglionic pacemaker driving islets to a preferred frequency, no neural circuitry for this pacemaker has been identified. In this study, both points are addressed using a microfluidic system that allows for the pulsed application of the muscarinic agonist carbachol. We find that murine islets are entrained and synchronized over a wide range of frequencies when the carbachol pulsing is periodic, adding support to the hypothesis that ganglia can synchronize islets in vivo. We also find that islet synchronization is very effective even if the carbachol pulses are applied at random times. This suggests that a neural pacemaker is not needed; all that is required is that islets receive occasional coordinated input from postganglionic neurons. The endogenous rhythmic activity of the islets then sets the frequency of the islet population rhythm, while the input from ganglia acts only to keep the islet oscillators in phase.
Psychoactive pollutants, such as antidepressants, are increasingly detected in the environment. Mounting evidence suggests that such pollutants can disrupt the behaviour of non-target species. ...Despite this, few studies have considered how the response of exposed organisms might be mediated by social context. To redress this, we investigated the impacts of two environmentally realistic concentrations of a pervasive antidepressant pollutant, fluoxetine, on foraging behaviour in fish (
), tested individually or in a group. Fluoxetine did not alter behaviour of solitary fish. However, in a group setting, fluoxetine exposure disrupted the frequency of aggressive interactions and food consumption, with observed effects being contingent on both the mean weight of group members and the level of within-group variation in weight. Our results suggest that behavioural tests in social isolation may not accurately predict the environmental risk of chemical pollutants for group-living species and highlight the potential for social context to mediate the effects of psychoactive pollutants in exposed wildlife.
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