Differences between individuals in behavioral type (i.e. animal personality) are ecologically and evolutionarily important because they can have significant effects on fitness components such as growth and predation risk. In the present study we are used the invasive round goby (Neogobius melanostomus) from an established population in controlled experiments to examine the relationships among personality, metabolic performance, and growth rate (inferred as size-at-age). Boldness was measured as the time to return to normal behavior after a simulated predator attack, where fish with shorter freezing times were categorized as "bold" and fish with longer times were categorized as "shy." We show that bold fish have significantly higher standard metabolic rate (SMR) than their shy conspecifics, whereas there was no difference between personality types in their maximum metabolic rate (MMR) or aerobic scope (AS). Bold fish furthermore had a smaller size-at-age as compared to shy fish. Together this provides evidence of a metabolic underpinning of personality where the high-SMR bold fish require more resources to sustain basic life functions than their low-SMR shy conspecifics, indicating that bold round goby from established populations with high densities (and high competition for food) pay a price of reduced growth rate.
This study examines the impact of boldness on foraging competition of the highly invasive round goby Neogobius melanostomus Pallas 1815. Individual risk tolerance, or boldness, was measured as the time to resume movement after a simulated predation strike. Fish that resumed movement faster were categorized as "bold," fish that took more time to resume movement were categorized as "shy" and those that fell in between these two categories were determined to have "intermediate" boldness. Competitive impacts of boldness in N. melanostomus were determined in a laboratory foraging experiment in which interspecific (juvenile Atlantic cod Gadus morhua Linnaeus 1758) and intraspecific (intermediate N. melanostomus) individuals were exposed to either bold or shy N. melanostomus competitors. G. morhua consumed fewer prey when competing with bold N. melanostomus than when competing with shy N. melanostomus, whereas intermediately bold N. melanostomus foraging was not affected by competitor boldness. Bold and shy N. melanostomus consumed similar amounts of prey, and the number of interactions between paired fish did not vary depending on the personality of N. melanostomus individuals. Therefore, intraspecific foraging competition was not found to be personality dependent. This study provides evidence that individual differences in boldness can mediate competitive interactions in N. melanostomus; nonetheless, results also show that competition is also governed by other mechanisms that require further study.
Production and human consumption of pharmaceuticals result in contamination of surface waters worldwide. Little is known about the long-term (i.e., over decades) fate of pharmaceuticals in aquatic systems. Here, we show that the most prescribed anxiolytic in Sweden (oxazepam) persists in its therapeutic form for several decades after being deposited in a large freshwater lake. By comparing sediment cores collected in 1995 and 2013, we demonstrate that oxazepam inputs from the early 1970s remained in the sediments until sampling in 2013, despite in situ degradation processes and sediment diagenesis. In laboratory and pond experiments, we further reveal that therapeutic forms of oxazepam can persist over several months in cold (5 degrees C) lake water free from UV light. We conclude that oxazepam can persist in lakes over a time scale much longer than previously realized and that levels can build up in lakes due to both a legacy of past inputs and a growing urban population.
Standardized ecotoxicological tests still constitute the fundamental tools when doing risk-assessment of aquatic contaminants. These protocols are managed towards minimal mortality in the controls, which is not representative for natural systems where mortality is often high. This methodological bias, generated from assays where mortality in the control group is systematically disregarded, makes it difficult to measure therapeutic effects of pharmaceutical contaminants leading to lower mortality. This is of concern considering that such effects on exposed organisms still may have substantial ecological consequences. In this paper, we illustrate this conceptual problem by presenting empirical data for how the therapeutic effect of Oxazepam-a common contaminant of surface waters-lower mortality rates among exposed Eurasian perch (Perca fluviatilis) from wild populations, at two different life stages. We found that fry hatched from roe that had been exposed to dilute concentrations (1.1 +/- 0.3 mu g l(-1)) of Oxazepam for 24 h 3-6 days prior to hatching showed lower mortality rates and increased activity 30 days after hatching. Similar effects, i.e. increased activity and lower mortality rates were also observed for 2-year old perch exposed to dilute Oxazepam concentrations (1.2 +/- 0.4 mu g l(-1)). We conclude that therapeutic effects from pharmaceutical contaminants need to be considered in risk assessment assays to avoid that important ecological effects from aquatic contaminants are systematically missed.
Pharmaceutical active compounds (PhACs) are increasingly being reported in wastewater effluents and surface waters around the world. The presence of these products, designed to modulate human physiology and behaviour, has created concern over whether PhACs similarly affect aquatic organisms. Though laboratory studies are beginning to address the effects of individual PhACs on fish behaviour, few studies have assessed the effects of exposure to complex, realistic wastewater effluents on fish behaviour. In this study, we exposed a wild, invasive fish species—the round goby (Neogobius melanostomus)—to treated wastewater effluent (0%, 50% or 100% effluent dilutions) for 28 days. We then determined the impact of exposure on fish aggression, an important behaviour for territory acquisition and defense. We found that exposure to 100% wastewater effluent reduced the number of aggressive acts that round goby performed. We complimented our behavioural assay with measures of pharmaceutical uptake in fish tissues. We detected 11 of 93 pharmaceutical compounds that we tested for in round goby tissues, and we found that concentration was greatest in the brain followed by plasma, then gonads, then liver, and muscle. Fish exposed to 50% and 100% effluent had higher tissue concentrations of pharmaceuticals and concentrated a greater number of pharmaceutical compounds compare to control fish exposed to no (0%) effluent. Exposed fish also showed increased ethoxyresorufin-O-deethylase (EROD) activity in liver tissue, suggesting that fish were exposed to planar halogenated/polycyclic aromatic hydrocarbons (PHHs/PAHs) in the wastewater effluent. Our findings suggest that fish in effluent-dominated systems may have altered behaviours and greater tissue concentration of PhACs. Moreover, our results underscore the importance of characterizing exposure to multiple pollutants, and support using behaviour as a sensitive tool for assessing animal responses to complex contaminant mixtures, like wastewater effluent.
Pharmaceuticals entering aquatic ecosystems via wastewater effluents are of increasing concern for wild animals. Because some pharmaceuticals are designed to modulate human behaviour, measuring the impacts of exposure to pharmaceuticals on fish behaviour has become a valuable endpoint. While laboratory studies have shown that pharmaceuticals can affect fish behaviour, there is a lack of understanding if behaviour is similarly affected in natural environments. Here, we exposed sea trout (Salmo trutta) smolts to two concentrations of two pharmaceutical pollutants often detected in surface waters: temazepam (a benzodiazepine, anxiolytic) or irbesartan (an angiotensin II receptor blocker, anti-hypertensive). We tested the hypothesis that changes to behavioural traits (anxiety and activity) measured in laboratory trials following exposure are predictive of behaviour in the natural environment (downstream migration). Measures of anxiety and activity in the laboratory assay did not vary with temazepam treatment, but temazepam-exposed fish began migrating faster in the field. Activity in the laboratory assay did predict overall migration speed in the field. In contrast to temazepam, we found that irbesartan exposure did not affect behaviour in the laboratory, field, or the relationship between the two end-points. However, irbesartan was also not readily taken up into fish tissue (i.e. below detection levels in the muscle tissue), while temazepam bioconcentrated (bioconcentration factor 7.68) rapidly (t(1/2) < 24 h). Our findings add to a growing literature showing that benzodiazepine pollutants can modulate fish behaviour and that laboratory assays may be less sensitive at detecting the effects of pollutants compared to measuring effects in natural settings. Therefore, we underscore the importance of measuring behavioural effects in the natural environment.
A multitude of biologically active pharmaceuticals contaminate surface waters globally, yet their presence in aquatic food webs remain largely unknown. Here, we show that over 60 pharmaceutical compounds can be detected in aquatic invertebrates and riparian spiders in six streams near Melbourne, Australia. Similar concentrations in aquatic invertebrate larvae and riparian predators suggest direct trophic transfer via emerging adult insects to riparian predators that consume them. As representative vertebrate predators feeding on aquatic invertebrates, platypus and brown trout could consume some drug classes such as antidepressants at as much as one-half of a recommended therapeutic dose for humans based on their estimated prey consumption rates, yet the consequences for fish and wildlife of this chronic exposure are unknown. Overall, this work highlights the potential exposure of aquatic and riparian biota to a diverse array of pharmaceuticals, resulting in exposures to some drugs that are comparable to human dosages.