Differential effects of parental and developmental temperatures on larval thermal adaptation in oviparous and viviparous model fish species.

Phenotypic plasticity has been identified as a major mechanism of response to changing temperatures. Parental effects are potentially important drivers of ecological and evolutionary dynamics, while developmental plasticity also plays a key role in generating phenotypic variation. However, little is known of the interaction between parental effects and developmental plasticity on the thermal phenotypes of fishes with different reproductive modes (i.e. oviparous vs. viviparous). To understand the contributions of inter- and intra-generational plasticity of thermal phenotypes (preferred temperature, avoidance temperatures, critical thermal thresholds) in fishes with different reproductive modes, we carried out a factorial experiment in which both breeding parents and offspring were exposed to lower (22 °C) or higher (28 °C) temperatures, using zebrafish (Danio rerio) and guppies (Poecilia reticulata) as representative oviparous and viviparous species. We found that offspring thermal preference and avoidance of both species were significantly influenced by parental effects and developmental plasticity, with higher thermal preference and avoidance consistent with higher background (parental) temperature treatments. However, parental effects were only found to impose significant effect on the thermal tolerances of guppies. The findings suggest that phenotypic plasticity, both within and across generations, may be an important mechanism to adapt to rapid climate changes, and that future temperature fluctuations may impose more profound effects on viviparous fish species in general.

A field test of the "graveyard hypothesis" reveals avoidance of chemical but not visual cues in Bahamian queen conch (Aliger gigas).

Queen conch (Aliger gigas) are large gastropod molluscs harvested for their meat, shells, and pearls and as they are generally easy to collect by hand, they are vulnerable to overfishing. In The Bahamas, fishers often clean (or "knock") their catch and dispose of the shells away from collection sites, forming midden heaps or "graveyards". Although queen conch are motile and found throughout shallow water habitats, live animals are rarely observed in the vicinity of middens, giving rise to a common belief that conch actively avoid graveyards, possibly by moving offshore. Here, we experimentally evaluated avoidance behaviours of queen conch to chemical (tissue homogenate) and visual (shells) cues indicative of harvesting activity using replicated aggregations of six size-selected small (< 14 cm shell length) and large (> 14 cm) conch at Eleuthera Island. Large conch were consistently more likely to move, and to move farther, than small conch, independent of treatment. Small conch, however, demonstrated greater occurrence of movement in response to chemical cues vs seawater controls, while conch of both sizes demonstrated equivocal responses to visual cues. Collectively, these observations suggest that more economically desirable large conch may be less vulnerable to capture during successive harvest events than smaller juveniles due to their greater propensity to move, and that chemical cues consistent with damage-released alarm cues may play a greater role in eliciting avoidance behaviour than the visual cues typically associated with queen conch graveyards. DATA AVAILABILITY: Data and R code are archived and freely available at Open Science Framework (https://osf.io/x8t7p/; DOI: 10.17605/OSF.IO/X8T7P).

Metabolic constraints and individual variation shape the trade-off between physiological recovery and anti-predator responses in adult sockeye salmon.

Metabolic scope represents the aerobic energy budget available to an organism to perform non-maintenance activities (e.g., escape a predator, recover from a fisheries interaction, compete for a mate). Conflicting energetic requirements can give rise to ecologically relevant metabolic trade-offs when energy budgeting is constrained. The objective of this study was to investigate how aerobic energy is utilized when individual sockeye salmon (Oncorhynchus nerka) are exposed to multiple acute stressors. To indirectly assess metabolic changes in free-swimming individuals, salmon were implanted with heart rate biologgers. The animals were then exercised to exhaustion or briefly handled as a control, and allowed to recover from this stressor for 48 h. During the first 2 h of the recovery period, individual salmon were exposed to 90 ml of conspecific alarm cues or water as a control. Heart rate was recorded throughout the recovery period. Recovery effort and time was higher in exercised fish, relative to control fish, whereas exposure to an alarm cue had no effect on either of these metrics. Individual routine heart rate was negatively correlated with recovery time and effort. Together, these findings suggest that metabolic energy allocation towards exercise recovery (i.e., an acute stressor; handling, chase, etc.) trumps anti-predator responses in salmon, although individual variation may mediate this effect at the population level.

Chemical communication in wood frog (Rana sylvatica) tadpoles is influenced by early-life exposure to naphthenic acid fraction compounds.

Environmental pollutants can disrupt chemical communication between aquatic organisms by interfering with the production, transmission, and/or detection of, as well as responses to, chemical cues. Here, we test the hypothesis that early-life exposure to naphthenic acid fraction compounds (NAFCs) from oil sands tailings disrupts antipredator-associated chemical communication in larval amphibians. Wild adult wood frogs (Rana sylvatica) captured during their natural breeding period were combined (1 female:2 males) in six replicate mesocosms filled with either uncontaminated lakewater or with NAFCs isolated from an active tailings pond in Alberta, Canada, at nominal 5 mg/L concentrations. Egg clutches were incubated and tadpoles maintained in their respective mesocosms for ∼40 days post-hatch. Tadpoles (Gosner stage 25-31) were then transferred individually to trial arenas filled with uncontaminated water and exposed to one of six chemical alarm cue (AC) stimuli solutions following a 3 × 2 × 2 design (3 AC types × 2 stimulus carriers × 2 rearing exposure groups). Relative to control tadpoles, NAFC-exposed tadpoles demonstrated higher baseline activity levels (line crosses and direction changes) when introduced to uncontaminated water. Antipredator responses differed in graded fashion with AC type, with control ACs eliciting the greatest latency to resume activity, water the least, and NAFC-exposed ACs intermediate. Pre- to post-stimulus difference scores were non-significant in control tadpoles, while NAFC-exposed tadpoles demonstrated significantly greater variation. While this suggests that exposure to NAFCs from fertilization through hatching may have interfered with AC production, it is unclear whether the quality or quantity of cues was affected. There was also no clear evidence that NAFC carrier water interfered with ACs or the alarm response in unexposed control tadpoles. These results emphasize the importance of understanding how behavioral and physiological effects of early-life NAFC exposure on critical antipredator responses may persist across life history stages.

No evidence for collateral effects of electromagnetic fields used to increase dissolved oxygen levels on the behavior and physiology of freshwater fishes.

Hypoxia in surface waters driven by warming climate and other anthropogenic stressors is a major conservation concern, and technological solutions for water quality remediation are sorely needed. One potential solution involves the use of low-intensity electromagnetic fields (EMFs) to increase dissolved oxygen levels, but potential collateral effects of the EMFs on aquatic animals have not been formally evaluated. We examined the effects of EMF exposure on wild-caught, captive sunfish (Lepomis spp.) over 8-day and 3-day exposures, with and without aeration in mesocosms and stock tanks (respectively). We also quantified ambient fish abundance in close proximity to EMF devices deployed in Opinicon Lake (ON). We found no significant differences in a suite of blood-based stress physiology biomarkers, behaviors, and putative aerobic capacities between EMF and control conditions over 8 days. Aerated mesocosms equipped with activated EMFs consistently had higher oxygen levels in the water than aerated controls. There were no differences in mortality during 3-day oxygen depletion trials under EMF or control conditions, and we detected no differences in fish abundance when the devices were activated in the lake. Our findings suggest that deploying EMF devices in field settings is not likely to exert negative effects on exposed fish populations. PRACTITIONER POINTS: Low-cost, low-energy technological solutions to remediate aquatic hypoxia are sorely needed Electromagnetic fields (EMFs) can increase oxygen flux across air/water interfaces and increase dissolved oxygen levels We found no evidence of negative effects of EMFs on fish physiology or behavior and our results support their use in alleviating hypoxic conditions.

Fathead Minnows Exposed to Organic Compounds from Oil Sands Tailings as Embryos Have Reduced Survival, Impaired Development, and Altered Behaviors That Persist into Larval Stages.

Our study evaluated whether exposure to naphthenic acid fraction compounds (NAFCs) extracted from oil sands process-affected waters (OSPW) has adverse effects on fish embryos that persist into later life. We exposed fathead minnow (Pimephales promelas) embryos to concentrations of NAFCs found in OSPW (2.5-54 mg/L) for 7 days (1 day postfertilization to hatch), then raised surviving larvae in outdoor mesocosms of uncontaminated lake water for 1 month. Embryos exposed to NAFCs were more likely to exhibit malformations (by up to 8-fold) and had slower heart rates (by up to 24%) compared to controls. Fish raised in uncontaminated lake water following exposure to NAFCs as embryos, were 2.5-fold less likely to survive during the larval stage than control fish. These fish also showed up to a 45% decrease in swim activity and a 36% increase in swim burst events during behavioral tests relative to controls. We conclude that exposure to NAFCs during the embryonic stage can have lasting effects on fish survival, physiology, and behavior that persist at least through the larval stage. These findings of delayed mortalities and persistent sublethal effects of embryonic NAFC exposure are relevant to informing the development of regulations on treated OSPW releases from mining operations. Environ Toxicol Chem 2022;41:1319-1332. © 2022 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

Exploiting common senses: sensory ecology meets wildlife conservation and management.

Multidisciplinary approaches to conservation and wildlife management are often effective in addressing complex, multi-factor problems. Emerging fields such as conservation physiology and conservation behaviour can provide innovative solutions and management strategies for target species and systems. Sensory ecology combines the study of 'how animals acquire' and process sensory stimuli from their environments, and the ecological and evolutionary significance of 'how animals respond' to this information. We review the benefits that sensory ecology can bring to wildlife conservation and management by discussing case studies across major taxa and sensory modalities. Conservation practices informed by a sensory ecology approach include the amelioration of sensory traps, control of invasive species, reduction of human-wildlife conflicts and relocation and establishment of new populations of endangered species. We illustrate that sensory ecology can facilitate the understanding of mechanistic ecological and physiological explanations underlying particular conservation issues and also can help develop innovative solutions to ameliorate conservation problems.

Acute warming in winter eliminates chemical alarm responses in threatened Qinling lenok Brachymystax lenok tsinlingensis.

Knowledge of how temperature influences animal behavior is critical to understanding and predicting impacts of changing climate on individual species and biotic interactions. However, the effects of climate change, especially winter warming in freshwater systems, on fish behaviors and the use of chemical information have been largely unexplored. Qinling lenok Brachymystax lenok tsinlingensis, an endangered salmonid species endemic to the Qinling Mountain Range, China, is currently experiencing population decline and is a potential biological indicator of warming winter climate effects on freshwater fishes due to its temperature sensitivity and required habitat of small, cold-water streams. Our objective was to determine if transient winter warming (increases of ~4 °C) consistent with seasonal maxima in line with near-future climate projections will affect antipredator responses to damage-released chemical alarm cues in B. lenok tsinlingensis. Wild fish were collected during winter and held in captivity under food deprivation for four days, during which half were acclimated to a warmer temperature (6 °C) while the other half were maintained at ambient levels (2 °C). Individual acclimated fish were then exposed to injections of either conspecific alarm cues to simulate elevated predation risk or stream water as a control treatment. Focal fish demonstrated responses consistent with antipredator behaviors to alarm cues at ambient temperature, but no significant behavioral responses to alarm cues were found relative to controls at the warmer temperature. These results support our hypothesis that winter warming will negatively influence antipredator responses and indicate that projected warmer temperature patterns in winter may have significant impacts on chemically mediated predator-prey interactions in cold-water streams.

Predation risk mediates cognitive constraints following physical exertion in schoolmaster snapper.

A large body of literature suggests that physically exhausted fish, including those that are released following fisheries interactions, experience behavioural and cognitive constraints and are at elevated risk of predation during homeostatic recovery. However, previous studies have focused on exhausted fish subsequently encountering predators, and not on fish that had been exposed to elevated predation risk prior to exhaustive exercise. Here, we exercised individual schoolmaster snapper (Lutjanus apodus) for 0, 1, or 4 min via hand chases following exposure to conspecific chemical alarm cues or seawater controls. The snapper were then introduced into one end of a rectangular arena supplied with mangrove prop roots as a refuge at the opposite end. Snapper exposed to the seawater control treatment demonstrated graded responses in mean times to move one body length and latency to enter the refuge, with unchased fish taking the least time and fish chased for 4 mins taking the longest. Amongst the snapper pre-exposed to alarm cues, the graded response did not occur and mean responses did not differ between chase treatments. Consistent with increased antipredator vigilance, alarm cue-exposed snapper were more likely to subsequently exit the refuge and to do so more times than fish exposed to seawater controls, independent of chase time. These observations suggest that perception of elevated predation risk may induce a conditional response offseting the behavioural and cognitive constraints associated with physical exhaustion through an unknown physiological mechanism to prioritize immediate survival-oriented behaviours over recovery.

Coloured LED light as a potential behavioural guidance tool for age 0 and 2 year walleye Sander vitreus.

Based on existing laboratory research on the visual physiology of walleye Sander vitreus, we tested colours of known spectral sensitivity (i.e., green and orange) using constant and strobing (5 Hz) illumination with an LED-based light guidance device (LGD). Hatchery-reared age 0 and 2 years S. vitreus were exposed to these four light combinations as well as an unilluminated control treatment during day and night trials. Age 2 years S. vitreus generally avoided the LGD when light was produced (negative phototaxis) compared with the control, with continuous illumination having a greater effect than strobing. The proportions of both age 0 and 2 year fish exiting illuminating zones of the trial arena did not differ with light colour or strobe rate, suggesting that phototactic behaviours in S. vitreus do not change with ontogeny in these age classes. Our findings confirm that typical behavioural responses of S. vitreus to light stimuli are characterised by avoidance and provide evidence that the use of light for behavioural guidance (deterrence) may be effective at reducing entrainment and impingement of this species on hydraulic barriers during migrations, independent of ontogenetic stage.

Impacts of Channel Morphodynamics on Fish Habitat Utilization.

It is reasonable to expect that hydro-morphodynamic processes in fluvial systems can affect fish habitat availability, but the impacts of morphological changes in fluvial systems on fish habitat are not well studied. Herein we investigate the impact of morphological development of a cohesive meandering stream on the quality of fish habitat available for juvenile yellow perch (Perca flavescens) and white sucker (Catostomus commersonii). A three-dimensional (3D) morphodynamic model was first developed to simulate the hydro-morphodynamics of the study creek. The results of the morphodynamic model were then incorporated into a fish habitat availability assessment. The 3D hydro-morphodynamic model was successfully calibrated using an intensive acoustic Doppler current profiler (ADCP) spatial survey of the entire 3D velocity field and total station surveys of topographic changes in a meander bend in the study creek. Two fish sampling surveys were carried out at the beginning and the end of the study period to determine presence-absence of fish as an indicator of the habitat utilization of each fish species in the study reach. It was shown that morphological development of the stream was a significant factor for the observed changes in the habitat utilization of juvenile yellow perch. It is shown that juvenile yellow perch mostly utilized habitat where deposition occurred whereas they avoided areas of erosion. The results of this study and the proposed methodology could provide some insights into the potential impact of sediment transport processes on the fish occurrence, and distribution and has implications for management of small fluvial systems.

Association Mapping Based on a Common-Garden Migration Experiment Reveals Candidate Genes for Migration Tendency in Brown Trout.

A better understanding of the environmental and genetic contribution to migratory behavior and the evolution of traits linked to migration is crucial for fish conservation and fisheries management. Up to date, a few genes with unequivocal influence on the adoption of alternative migration strategies have been identified in salmonids. Here, we used a common garden set-up to measure individual migration distances of generally highly polymorphic brown trout Salmo trutta from two populations. Fish from the assumedly resident population showed clearly shorter migration distances than the fish from the assumed migratory population at the ages of 2 and 3 years. By using two alternative analytical pipelines with 22186 and 18264 SNPs obtained through RAD-sequencing, we searched for associations between individual migration distance, and both called genotypes and genotype probabilities. None of the SNPs showed statistically significant individual effects on migration after correction for multiple testing. By choosing a less stringent threshold, defined as an overlap of the top 0.1% SNPs identified by the analytical pipelines, GAPIT and Angsd, we identified eight candidate genes that are potentially linked to individual migration distance. While our results demonstrate large individual and population level differences in migration distances, the detected genetic associations were weak suggesting that migration traits likely have multigenic control.

Interactive effects of reproductive assets and ambient predation risk on the threat-sensitive decisions of Trinidadian guppies.

Threat-sensitive behavioral trade-offs allow prey animals to balance the conflicting demands of successful predator detection and avoidance and a suite of fitness-related activities such as foraging, mating, and territorial defense. Here, we test the hypothesis that background predation level and reproductive status interact to determine the form and intensity of threat-sensitive behavioral decisions of wild-caught female Trinidadian guppies Poecilia reticulata. Gravid and nongravid guppies collected from high- and low-predation pressure populations were exposed to serial dilutions of conspecific chemical alarm cues. Our results demonstrate that there was `no effect of reproductive status on the response of females originating from a low-predation population, with both gravid and nongravid guppies exhibiting strong anti-predator responses to the lowest concentration of alarm cues tested. Increasing cue concentrations did not result in increases in response intensity. Conversely, we found a significant effect of reproductive status among guppies from a high-predation population. Nongravid females from the high-predation population exhibited a strong graded (proportional) response to increasing concentrations of alarm cue. Gravid females from the same high-predation population, however, shifted to a nongraded response. Together, these results demonstrate that accrued reproductive assets influence the threat-sensitive behavioral decisions of prey, but only under conditions of high-ambient predation risk.

Local predation risk shapes spatial and foraging neophobia patterns in Trinidadian guppies.

The "dangerous niche" hypothesis posits that neophobia functions to reduce the cost of habitat use among animals exposed to unknown risks. For example, more dangerous foraging or higher competition may lead to increased spatial neophobia. Likewise, elevated ambient predation threats have been shown to induce phenotypically plastic neophobic predator avoidance. In both cases, neophobia is argued to reduce the cost of living associated with ecological uncertainty. Here, we test the hypothesis that ambient predation shapes both neophobic predator avoidance and spatial and foraging neophobia in Trinidadian guppies. Guppies were exposed to a novel foraging arena paired with a known cue (conspecific alarm cue), a novel cue (lemon odor), or a stream water control in three streams differing in ambient predation risk. We demonstrate that guppies from a high-predation-risk stream exhibited risk-averse foraging patterns regardless of the chemical stimulus presented (high spatial neophobia) and that those from a low-predation-risk stream were only risk-averse when the foraging arenas were paired with conspecific alarm cue (lower spatial neophobia). Those tested in the intermediate-predation-risk stream were consistently intermediate to the high-risk vs. low-risk populations. Our study suggests that ambient predation risk shapes both neophobic predator avoidance and space-use patterns and that neophobia may function as a "generalized" response to ecological uncertainty.

Personality and the response to predation risk: effects of information quantity and quality.

Within aquatic ecosystems, chemosensory cues provide valuable public information regarding the form and degree of risk, allowing prey to make informed behavioural decisions. Such cues, however, may vary in both relative concentration detected (i.e. 'quantity') and reliability of the information available (i.e. 'quality'), leading to varying response patterns. Moreover, prey species are also known to exhibit consistent behavioural tactics towards managing risk (i.e. personality), possibly shaping their use of public information. Here, we present two experiments examining the potential interacting effects of personality and the quantity (Experiment 1) or quality (Experiment 2) of public information on the short-term predator avoidance responses of wild-caught Trinidadian guppies under semi-natural conditions. Our first experiment demonstrated that personality shaped responses to a high concentration of alarm cues (high risk), with shyer guppies exhibiting stronger antipredator responses than bolder guppies. When exposed to either low risk or stream water controls, personality had no effect on the intensity of response. Our second experiment demonstrated that personality again shaped the response to high concentrations of alarm cues (a known risk) but not to a novel chemosensory cue (tilapia odour). When exposed to the unknown novel cue, guppies exhibited a relatively high intensity antipredator response, regardless of personality. Combined, our results suggest that individual risk-taking tactics shape the use of public information in a context-dependent fashion.

Phenotypically plastic neophobia: a response to variable predation risk.

Prey species possess a variety of morphological, life history and behavioural adaptations to evade predators. While specific evolutionary conditions have led to the expression of permanent, non-plastic anti-predator traits, the vast majority of prey species rely on experience to express adaptive anti-predator defences. While ecologists have identified highly sophisticated means through which naive prey can deal with predation threats, the potential for death upon the first encounter with a predator is still a remarkably important unresolved issue. Here, we used both laboratory and field studies to provide the first evidence for risk-induced neophobia in two taxa (fish and amphibians), and argue that phenotypically plastic neophobia acts as an adaptive anti-predator strategy for vulnerable prey dealing with spatial and temporal variation in predation risk. Our study also illustrates how risk-free maintenance conditions used in laboratory studies may blind researchers to adaptive anti-predator strategies that are only expressed in high-risk conditions.

Understanding the importance of episodic acidification on fish predator-prey interactions: does weak acidification impair predator recognition?

The ability of prey to recognize predators is a fundamental prerequisite to avoid being eaten. Indeed, many prey animals learn to distinguish species that pose a threat from those that do not. Once the prey has learned the identity of one predator, it may generalize this recognition to similar predators with which the prey has no experience. The ability to generalize reduces the costs associated with learning and further enhances the ability of the prey to avoid relevant threats. For many aquatic organisms, recognition of predators is based on odor signatures, consequently any anthropogenic alteration in water chemistry has the potential to impair recognition and learning of predators. Here we explored whether episodic acidification could influence the ability of juvenile rainbow trout to learn to recognize an unknown predator and then generalize this recognition to a closely related predator. Trout were conditioned to recognize the odor of pumpkinseed sunfish under circumneutral (~pH 7) conditions, and then tested for recognition of pumpkinseed or longear sunfish under both neutral or weakly acidic (~pH 6) conditions. When tested for a response to pumpkinseed odor, we found no significant effect of predator odor pH: trout responded similarly regardless of pH. Moreover, under neutral conditions, trout were able to generalize their recognition to the odor of longear sunfish. However, the trout could not generalize their recognition of the longear sunfish under acidic conditions. Given the widespread occurrence of anthropogenic acidification, acid-mediated impairment of predator recognition and generalization may be a pervasive problem for freshwater salmonid populations and other aquatic organisms.