Maze design: size and number of choices impact fish performance in cognitive assays.

Although studies on fish cognition are increasing, consideration of how methodological details influence the ability to detect and measure performance is lagging. Here, in two separate experiments the authors compared latency to leave the start position, latency to make a decision, levels of participation and success rates (whether fish entered the rewarded chamber as first choice) across different physical designs. Experiments compared fish performance across (a) two sizes of T-mazes, large and standard, and a plus-maze, and (b) open choice arenas with either two or four doors. Fish in T-mazes with longer arms took longer to leave the start chamber and were less likely to participate in a trial than fish in T-mazes with shorter arms. The number of options, or complexity, in a maze significantly impacted success but did not necessarily impact behavioural measures, and did not impact the number of fish that reached a chamber. Fish in the plus-maze had similar latencies to leave the start box and time to reach any chamber as fish in the same-sized T-maze but exhibited lower overall success. Similarly, in an open choice arena, increasing the number of options - doors to potential reward chambers - resulted in lower probability of success. There was an influence of reward position in the choice arena, with rewarded chambers closest to the sides of the arena resulting in lower latencies to enter and higher probability of decision success. Together the results allow the authors to offer practical suggestions towards optimal maze design for studies of fish cognition.

The role of vital dietary biomolecules in eco-evo-devo dynamics.

The physiological dependence of animals on dietary intake of vitamins, amino acids, and fatty acids is ubiquitous. Sharp differences in the availability of these vital dietary biomolecules among different resources mean that consumers must adopt a range of strategies to meet their physiological needs. We review the emerging work on omega-3 long-chain polyunsaturated fatty acids, focusing predominantly on predator-prey interactions, to illustrate that trade-off between capacities to consume resources rich in vital biomolecules and internal synthesis capacity drives differences in phenotype and fitness of consumers. This can then feedback to impact ecosystem functioning. We outline how focus on vital dietary biomolecules in eco-eco-devo dynamics can improve our understanding of anthropogenic changes across multiple levels of biological organization.

Linking omega-3 polyunsaturated fatty acids in natural diet with brain size of wild consumers.

Omega-3 long-chain polyunsaturated fatty acids (n-3 LC-PUFA) are key structural lipids and their dietary intake is essential for brain development of virtually all vertebrates. The importance of n-3 LC-PUFA has been demonstrated in clinical and laboratory studies, but little is known about how differences in the availability of n-3 LC-PUFA in natural prey influence brain development of wild consumers. Consumers foraging at the interface of aquatic and terrestrial food webs can differ substantially in their intake of n-3 LC-PUFA, which may lead to differences in brain development, yet this hypothesis remains to be tested. Here we use the previously demonstrated shift towards higher reliance on n-3 LC-PUFA deprived terrestrial prey of native brown trout Salmo trutta living in sympatry with invasive brook trout Salvelinus fontinalis to explore this hypothesis. We found that the content of n-3 LC-PUFA in muscle tissues of brown trout decreased with increasing consumption of n-3 LC-PUFA deprived terrestrial prey. Brain volume was positively related to the content of the n-3 LC-PUFA, docosahexaenoic acid, in muscle tissues of brown trout. Our study thus suggests that increased reliance on diets low in n-3 LC-PUFA, such as terrestrial subsidies, can have a significant negative impact on brain development of wild trout. Our findings provide the first evidence of how brains of wild vertebrate consumers response to scarcity of n-3 LC-PUFA content in natural prey.

Assessment of Compound-Specific Fatty Acid δ13C and δ2H Values to Track Fish Mobility in a Small Sub-alpine Catchment.

Methods for identifying origin, movement, and foraging areas of animals are essential for understanding ecosystem connectivity, nutrient flows, and other ecological processes. Telemetric methods can provide detailed spatial coverage but are limited to a minimum body size of specimen for tagging. In recent years, stable isotopes have been increasingly used to track animal migration by linking landscape isotope patterns into movement (isoscapes). However, compared to telemetric methods, the spatial resolution of bulk stable isotopes is low. Here, we examined a novel approach by evaluating the use of compound-specific hydrogen and carbon stable isotopes of fatty acids (δ2HFA and δ13CFA) from fish liver, muscle, brain, and eye tissues for identifying site specificity in a 254 km2 sub-alpine river catchment. We analyzed 208 fish (European bullhead, rainbow trout, and brown trout) collected in 2016 and 2018 at 15 different sites. δ13CFA values of these fish tissues correlated more among each other than those of δ2HFA values. Both δ2HFA and δ13CFA values showed tissue-dependent isotopic fractionation, while fish taxa had only small effects. The highest site specificity was for δ13CDHA values, while the δ2H isotopic difference between linoleic acid and alpha-linolenic acid resulted in the highest site specificity. Using linear discrimination analysis of FA isotope values, over 90% of fish could be assigned to their location of origin; however, the accuracy dropped to about 56% when isotope data from 2016 were used to predict the sites for samples collected in 2018, suggesting temporal shifts in site specificity of δ2HFA and δ13CFA. However, the predictive power of δ2HFA and δ13CFA over this time interval was still higher than site specificity of bulk tissue isotopes for a single time point. In summary, compound-specific isotope analysis of fatty acids may become a highly effective tool for assessing fine and large-scale movement and foraging areas of animals.

Differences in brain morphology of brown trout across stream, lake, and hatchery environments.

It has been suggested that a trade-off between cognitive capacity and developmental costs may drive brain size and morphology across fish species, but this pattern is less well explored at the intraspecific level. Physical habitat complexity has been proposed as a key selection pressure on cognitive capacity that shapes brain morphology of fishes. In this study, we compared brain morphology of brown trout, Salmo trutta, from stream, lake, and hatchery environments, which generally differ in physical complexity ranging from low habitat complexity in the hatchery to high habitat complexity in streams and intermediate complexity in lakes. We found that brain size, and the size of optic tectum and telencephalon differed across the three habitats, both being largest in lake fish with a tendency to be smaller in the stream compared to hatchery fish. Therefore, our findings do not support the hypothesis that in brown trout the volume of brain and its regions important for navigation and decision-making increases in physically complex habitats. We suggest that the observed differences in brain size might be associated with diet quality and habitat-specific behavioral adaptations rather than physical habitat complexity.

Asymmetric competition over space use and territory between native brown trout (Salmo trutta) and invasive brook trout (Salvelinus fontinalis).

Interference competition over food and territory can shape population structure and habitat use within and between species. The introduction of invasive species often leads to novel competitive interactions over shared resources and invaders can eventually exclude the native species from preferred habitats. Invasive brook trout (Salvelinus fontinalis) introduced to northern Europe have excluded native brown trout (Salmo trutta) from numerous headwater streams. The fact that invasive brook trout can displace the more aggressive brown trout is puzzling. However, the earlier spawning and hatching of brook trout, compared to brown trout, may lead to unequal competition due to size advantage and prior resident status of brook trout at the fry stage. In this study, we examine the effect of competition between brown trout and brook trout using the natural size distribution of the two species. In two consecutive experiments, we first measured space use and feeding of a fry (age 0+) in the presence of a juvenile (age 1+). In experiment 2, we assessed territorial interactions between the species at the fry stage (age 0+) and if smaller brown trout could compensate the disadvantage by manipulating residence duration. Fry of brook trout feed sooner and spend more time close to the larger individual than brown trout fry. We also found that brook trout fry won most territorial contests against brown trout, and that increased residence duration led to longer and more aggressive interactions. The results suggest that smaller brown trout are displaced to suboptimal habitats in the presence of a larger brook trout. Therefore, the later emergence from gravel beds resulting in the naturally occurring size disadvantage of brown trout at the fry stage may lead to unequal territorial interactions that could explain why brown trout are displaced from preferred habitats in sympatry with brook trout.

Growth-enhanced salmon modify stream ecosystem functioning.

Use of fast-growing domesticated and/or genetically modified strains of fish is becoming increasingly common in aquaculture, increasing the likelihood of deliberate or accidental introductions into the wild. To date, their ecological impacts on ecosystems remain to be quantified. Here, using a controlled phenotype manipulation by implanting growth hormone in juvenile Atlantic salmon (Salmo salar), we found that growth-enhanced fish display changes in several phenotypic traits known to be important for ecosystem functioning, such as habitat use, morphology and excretion rate. Furthermore, these phenotypic changes were associated with significant impacts on the invertebrate community and key stream ecosystem functions such as primary production and leaf-litter decomposition. These findings provide novel evidence that introductions of growth-enhanced fish into the wild can affect the functioning of natural ecosystems and represent a form of intraspecific invasion. Consequently, environmental impact assessments of growth-enhanced organisms need to explicitly consider ecosystem-level effects.

Guidelines for reporting methods to estimate metabolic rates by aquatic intermittent-flow respirometry.

Interest in the measurement of metabolic rates is growing rapidly, because of the importance of metabolism in advancing our understanding of organismal physiology, behaviour, evolution and responses to environmental change. The study of metabolism in aquatic animals is undergoing an especially pronounced expansion, with more researchers utilising intermittent-flow respirometry as a research tool than ever before. Aquatic respirometry measures the rate of oxygen uptake as a proxy for metabolic rate, and the intermittent-flow technique has numerous strengths for use with aquatic animals, allowing metabolic rate to be repeatedly estimated on individual animals over several hours or days and during exposure to various conditions or stimuli. There are, however, no published guidelines for the reporting of methodological details when using this method. Here, we provide the first guidelines for reporting intermittent-flow respirometry methods, in the form of a checklist of criteria that we consider to be the minimum required for the interpretation, evaluation and replication of experiments using intermittent-flow respirometry. Furthermore, using a survey of the existing literature, we show that there has been incomplete and inconsistent reporting of methods for intermittent-flow respirometry over the past few decades. Use of the provided checklist of required criteria by researchers when publishing their work should increase consistency of the reporting of methods for studies that use intermittent-flow respirometry. With the steep increase in studies using intermittent-flow respirometry, now is the ideal time to standardise reporting of methods, so that - in the future - data can be properly assessed by other scientists and conservationists.

Omega-3 PUFA profoundly affect neural, physiological, and behavioural competences - implications for systemic changes in trophic interactions.

In recent decades, much conceptual thinking in trophic ecology has been guided by theories of nutrient limitation and the flow of elements, such as carbon and nitrogen, within and among ecosystems. More recently, ecologists have also turned their attention to examining the value of specific dietary nutrients, in particular polyunsaturated fatty acids (PUFA), among which the omega-3 PUFA, especially eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) play a central role as essential components of neuronal cell membranes in many organisms. This review focuses on a new neuro-ecological approach stemming from the biochemical (mechanistic) and physiological (functional) role of DHA in neuronal cell membranes, in particular in conjunction with G-protein coupled receptors (GPCRs). We link the co-evolution of these neurological functions to metabolic dependency on dietary omega-3 PUFA. We outline ways in which deficiencies in dietary DHA supply may affect, cognition, vision, and behaviour, and ultimately, the biological fitness of consumers. We then review emerging evidence that changes in access to dietary omega-3 PUFA may ultimately have profound impacts on trophic interactions leading to potential changes in community structure and ecosystem functioning that, in turn, may affect the supply of DHA within and across ecosystems, including the supply for human consumption.

Reduced exploration capacity despite brain volume increase in warm-acclimated common minnow.

While evidence suggests that warming may impact cognition of ectotherms, the underlying mechanisms remain poorly understood. A possible but rarely considered mechanism is that the metabolic response of ectotherms to warming is associated with changes in brain morphology and function. Here, we compared aerobic metabolism, brain volume, boldness and accuracy of maze solving of common minnows (Phoxinus phoxinus) acclimated for 8 months to either their current optimal natural (14°C) or warm (20°C) water temperature. Metabolic rates indicated increased energy expenditure in warm-acclimated fish, but also at least partial thermal compensation as warm-acclimated fish maintained high aerobic scope. Warm-acclimated fish had larger brains than cool-acclimated fish. The volume of the dorsal medulla relative to the overall brain size was larger in warm- than in cool-acclimated fish, but the proportion of other brain regions did not differ between the temperature treatments. Warm-acclimated fish did not differ in boldness but made more errors than cool-acclimated fish in exploring the maze across four trials. Inter-individual differences in the number of exploration errors were repeatable across the four trials of the maze test. Our findings suggest that in warm environments, maintaining a high aerobic scope, which is important for the performance of physically demanding tasks, can come at the cost of changes in brain morphology and impairment of the capacity to explore novel environments. This trade-off could have strong fitness implications for wild ectotherms.

Phenotypic responses of invasive species to removals affect ecosystem functioning and restoration.

Reducing the abundances of invasive species by removals aims to minimize their ecological impacts and enable ecosystem recovery. Removal methods are usually selective, modifying phenotypic traits in the managed populations. However, there is little empirical evidence of how removal-driven changes in multiple phenotypic traits of surviving individuals of invasive species can affect ecosystem functioning and recovery. Overcoming this knowledge gap is highly relevant because individuals are the elemental units of ecological processes and so integrating individual-level responses into the management of biological invasions could improve their efficiency. Here we provide novel demonstration that removals by trapping, angling and biocontrol from lakes of the globally invasive crayfish Procambarus clarkii induced substantial changes in multiple phenotypic traits. A mesocosm experiment then revealed that these changes in phenotypic traits constrain recovery of basic ecosystem functions (decomposition of organic matter, benthic primary production) by acting in the opposite direction than the effects of reduced invader abundance. However, only minor ecological impacts of invader abundance and phenotypic traits variation remained a year after its complete eradication. Our study provides quantitative evidence to an original idea that removal-driven trait changes can dampen recovery of invaded ecosystems even when the abundance of invasive species is substantially reduced. We suggest that the phenotypic responses of invaders to the removal programme have strong effects on ecosystem recovery and should be considered within the management of biological invasions, particularly when complete eradication is not achievable.

The negative ecological impacts of a globally introduced species decrease with time since introduction.

While there is a long-history of biological invasions and their ecological impacts have been widely demonstrated across taxa and ecosystems, our knowledge on the temporal dynamic of these impacts remains extremely limited. Using a meta-analytic approach, we investigated how the ecological impacts of non-native brown trout (Salmo trutta), a model species with a 170-year-long and well-documented history of intentional introductions across the globe, vary with time since introduction. We first observed significant negative ecological impacts immediately after the species introduction. Second, we found that the negative ecological impacts decrease with time since introduction and that the average ecological impacts become nonsignificant more than one century after introduction. This pattern was consistent across other ecological contexts (i.e., geographical location, levels of biological organization, and methodological approach). However, overall negative ecological impacts were more pronounced at the individual and population levels and in experimental studies. While the mechanisms leading to this decrease remain to be determined, our results indicate that rapid response of native organisms (e.g. adaptation, but also local extinction) may play an important role in this dynamic. Changes in native species traits and local extinction can have important conservation implications. Therefore, we argue that the decline of the negative ecological impacts over time should not be used as an argument to neglect the negative impacts of biological invasions.

Behavioral type, in interaction with body size, affects the recapture rate of brown trout Salmo trutta juveniles in their nursery stream.

Movement activity levels of wild animals often differ consistently among individuals, reflecting different behavioral types. Previous studies have shown that laboratory-scored activity can predict several ecologically relevant characteristics. In an experiment on wild brown trout Salmo trutta, spanning from June to October, we investigated how spring swimming activity, measured in a standardized laboratory test, related to relative recapture probability in autumn. Based on laboratory activity scores, individuals clustered into 2 groups, which showed contrasting patterns in the size-dependency of their recapture probability. Size had a slightly positive effect on recapture probability for passive fish but a clear negative effect on active fish. Our results show that the population structure in a cohort, in terms of relative proportions of behavioral types in different size classes, can vary over time. The results of this study could depend on either selective mortality or migration. However, selective disappearance of individuals with specific phenotypes, regardless of the mechanism, will have implications for trout population management, such as stocking efficiency of hatchery fish with high growth rates or maintenance of fishways past migration barriers.

Encystment of parasitic freshwater pearl mussel (Margaritifera margaritifera) larvae coincides with increased metabolic rate and haematocrit in juvenile brown trout (Salmo trutta).

Gill parasites on fish are likely to negatively influence their host by inhibiting respiration, oxygen transport capacity and overall fitness. The glochidia larvae of the endangered freshwater pearl mussel (FPM, Margaritifera margaritifera (Linnaeus, 1758)) are obligate parasites on the gills of juvenile salmonid fish. We investigated the effects of FPM glochidia encystment on the metabolism and haematology of brown trout (Salmo trutta Linnaeus, 1758). Specifically, we measured whole-animal oxygen uptake rates at rest and following an exhaustive exercise protocol using intermittent flow-through respirometry, as well as haematocrit, in infested and uninfested trout. Glochidia encystment significantly affected whole-animal metabolic rate, as infested trout exhibited higher standard and maximum metabolic rates. Furthermore, glochidia-infested trout also had elevated levels of haematocrit. The combination of an increased metabolism and haematocrit in infested fish indicates that glochidia encystment has a physiological effect on the trout, perhaps as a compensatory response to the potential respiratory stress caused by the glochidia. When relating glochidia load to metabolism and haematocrit, fish with low numbers of encysted glochidia were the ones with particularly elevated metabolism and haematocrit. Standard metabolic rate decreased with substantial glochidia loads towards levels similar to those of uninfested fish. This suggests that initial effects visible at low levels of encystment may be countered by additional physiological effects at high loads, e.g. potential changes in energy utilization, and also that high numbers of glochidia may restrict oxygen uptake by the gills.

Inactive trout come out at night: behavioral variation, circadian activity, and fitness in the wild.

Theory suggests that high activity levels in animals increase growth at the cost of increased mortality. This growth-mortality tradeoff has recently been incorporated into the wider framework of the pace-of-life syndrome (POLS) hypothesis. However, activity is often quantified only in the laboratory and on a diurnal basis, leaving open the possibility that animals manage predation risk and feeding efficiency in the wild by modulating their circadian activity rhythms. Here we investigate how laboratory activity in wild brown trout parr (Salmo trutta L.) associates with circadian activity, growth, and mortality in their natal stream. We found that individuals with high activity in the laboratory displayed high dispersal and cathemeral activity in their natal stream. In contrast, trout with low laboratory activity showed variation of activity in the wild, which was negatively related to the light intensity. Our results do not support the growth-mortality trade-off of the POLS hypothesis as highly active, fast-growing individuals showed higher survival than inactive conspecifics. These novel results show for the first time that active and inactive individuals, as scored in the lab, can show different circadian patterns of behavior in the wild driven by light intensity. This implies that studies conducted under a narrow range of light conditions can bias our understanding of individual behavioral variation and its fitness consequences in the wild.

Energy costs of catfish space use as determined by biotelemetry.

Animals use dispersed resources within their home range (HR) during regular day-to-day activities. The high-quality area intensively used by an individual, where critical resources are concentrated, has been designated as the core area (CA). This study aimed to describe how animals utilize energy in the HR and CA assuming that changes would occur according to the size of the used areas. We observed energetic costs of space use in the largest European freshwater predator catfish, Silurus glanis, using physiological sensors. Catfish consumed significantly more energy within the CA compared to the rest of the HR area. In addition, energetic costs of space use within a large area were lower. These results generally indicate that utilization of larger areas is related to less demanding activities, such as patrolling and searching for new resources and mates. In contrast, fish occurrence in small areas appears to be related to energetically demanding use of spatially limited resources.