Joacim Näslund

Environmental effects on behavioural development consequences for fitness of captive-reared fishes in the wild

Why do captive-reared fishes generally have lower fitness in natural environments than wild conspecifics, even when the hatchery fishes are derived from wild parents from the local population? A thorough understanding of this question is the key to design artificial rearing environments that optimize post-release performance, as well as to recognize the limitations of what can be achieved by modifying hatchery rearing methods. Fishes are generally very plastic in their development and through gene-environment interactions, epigenetic and maternal effects their phenotypes will develop differently depending on their rearing environment. This suggests that there is scope for modifying conventional rearing environments to better prepare fishes for release into the wild. The complexity of the natural environment is impossible to mimic in full-scale rearing facilities. So, in reality, the challenge is to identify key modifications of the artificial rearing environment that are practically and economically feasible and that efficiently promote development towards a more wild-like phenotype. Do such key modifications really exist? Here, attempts to use physical enrichment and density reduction to improve the performance of hatchery fishes are discussed and evaluated. These manipulations show potential to increase the fitness of hatchery fishes released into natural environments, but the success is strongly dependent on adequately adapting methods to species and life stage-specific conditions.

Ghrelin increases food intake, swimming activity and growth in juvenile brown trout (Salmo trutta)

Several key functions of ghrelin are well conserved through vertebrate phylogeny. However, some of ghrelins effects are contradictory and among teleosts only a limited number of species have been used in functional studies on food intake and foraging-related behaviors. Here we investigated the long-term effects of ghrelin on food intake, growth, swimming activity and aggressive contest behavior in one year old wild brown trout (Salmo trutta) using intraperitoneal implants. Food intake and swimming activity were individually recorded starting from day 1, and aggressive behavior was tested at day 11, after ghrelin implantation. Body weight and growth rate were measured from the beginning to the end of the experiment. Triglycerides and lipase activity in muscle and liver; monoaminergic activity in the telencephalon and brainstem; and neuropeptide Y (NPY) mRNA levels in the hypothalamus were analyzed. Ghrelin treatment was found to increase food intake and growth without modifying lipid deposition or lipid metabolism in liver and muscle. Ghrelin treatment led to an increased foraging activity and a trend towards a higher swimming activity. Moreover, ghrelin-treated fish showed a tendency to initiate more conflicts, but this motivation was not reflected in a higher ability to win the conflicts. No changes were observed in monoaminergic activity and NPY mRNA levels in the brain. Ghrelin is therefore suggested to act as an orexigenic hormone regulating behavior in juvenile wild brown trout. These actions are accompanied with an increased growth without the alteration of liver and muscle lipid metabolism and they do not seem to be mediated by changes in brain monoaminergic activity or hypothalamic expression of NPY.

Density-Dependent Compensatory Growth in Brown Trout (Salmo trutta) in Nature

Density-dependence is a major ecological mechanism that is known to limit individual growth. To examine if compensatory growth (unusually rapid growth following a period of imposed slow growth) in nature is density-dependent, one-year-old brown trout (Salmo trutta L.) were first starved in the laboratory, and then released back into their natural stream, either at natural or at experimentally increased population density. The experimental trout were captured three times over a one-year period. We found no differences in growth, within the first month after release (May-June), between the starved fish and the control group (i.e. no evidence of compensation). During the summer however (July-September), the starved fish grew more than the control group (i.e. compensation), and the starved fish released into the stream at a higher density, grew less than those released at a natural density, both in terms of weight and length (i.e. density-dependent compensation). Over the winter (October-April), there were no effects of either starvation or density on weight and length growth. After the winter, starved fish released at either density had caught up with control fish in body size, but recapture rates (proxy for survival) did not indicate any costs of compensation. Our results suggest that compensatory growth in nature can be density-dependent. Thus, this is the first study to demonstrate the presence of ecological restrictions on the compensatory growth response in free-ranging animals.

Behavioural responses to simulated bird attacks in marine three-spined sticklebacks after exposure to high CO2 levels

The rising partial pressure of CO2 (pCO2) in oceanic water, termed ocean acidification, is an impending threat to marine life and has previously been reported to affect several aspects of fish behaviour. We evaluated the behavioural response to a simulated avian predator attack and lateralisation in three-spined sticklebacks (Gasterosteus aculeatus) after 10 and 20 days of exposure to present day pCO2 (400μatm) or elevated pCO2 (1000μatm). We show that elevated pCO2 lead to reduced behavioural lateralisation. However, no major differences in the sheltering response after an overhead avian attack were observed; fish from both treatments exhibited similar and strong responses. Compared with fish exposed to high pCO2, the control fish took longer time to freeze (i.e. stop moving) after attack at Day 20 but not Day 10. The freezing duration was significantly reduced between Day 10 and Day 20 in elevated pCO2, whereas no such reduction was observed in the control-group. However, no significant differences between treatment groups were detected at Day 20. These results demonstrate that behaviour is indeed altered by high CO2 levels, although the general responses to avian predation stimuli remain similar to those of unexposed fish, indicating that some predator avoidance behaviours of three-spined sticklebacks are robust to environmental disturbance.

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.

Co‐existence with non‐native brook trout breaks down the integration of phenotypic traits in brown trout parr

Summary A phenotypic syndrome refers to complex patterns of integration among functionally related traits in an organism that defines how the organism interacts with its environment and sustains itself. Human-induced biological invasions have become important sources of environmental modifications. However, the extent to which invasive species affect the phenotypic syndromes of individuals in a native is currently unknown. Such knowledge has important implications for understanding ecological interactions and the management of biological invasions. Here, field monitoring in a natural stream were combined with standardized estimates of behavioral, physiological and morphological traits to address the hypothesis that coexistence with a non-native invader induces a novel environmental pressure that disrupts the adaptive integration among phenotypic traits of the native species. We compared the strength of integration among key phenotypic traits (i.e. aerobic scope, standard metabolic rate, body growth, activity, and body shape) and ecological niche traits (i.e. spring and summer diet, home range size, daily movements) of an allopatric group of native brown trout (Salmo trutta) with a group of brown trout living in sympatry with non-native brook trout (Salvelinus fontinalis). We found that the integration of phenotypic traits was substantially reduced in the sympatric brown trout and that allopatric and sympatric brown trout differed in key phenotypic and ecological niche traits. Brown trout living in sympatry with non-native brook trout consumed more terrestrial prey, had smaller home ranges, and a stouter body shape. Sympatric brown trout also had lower specific growth rate, suggesting a lower fitness. The results are generally in line with our hypothesis suggesting that the reduction in fitness observed in sympatric brown trout is caused by the breakdown of their adaptive phenotypic syndrome. This may be caused by differences in the plasticity of the response of phenotypic traits to the novel selection pressure induced by the non-native species. Our results may help explaining deleterious effects of non-native species reported in the absence of direct competition with the native species. A lay summary is available for this article.

A simple non-invasive method for measuring gross brain size in small live fish with semi-transparent heads

This paper describes a non-invasive method for estimating gross brain size in small fish with semi-transparent heads, using system camera equipment. Macro-photographs were taken from above on backlit free-swimming fish undergoing light anaesthesia. From the photographs, the width of the optic tectum was measured. This measure (TeO-measure) correlates well with the width of the optic tectum as measured from out-dissected brains in both brown trout fry and zebrafish (Pearson r > 0.90). The TeO-measure also correlates well with overall brain wet weight in brown trout fry (r = 0.90), but less well for zebrafish (r = 0.79). A non-invasive measure makes it possible to quickly assess brain size from a large number of individuals, as well as repeatedly measuring brain size of live individuals allowing calculation of brain growth.

Cardiac remodeling and increased central venous pressure underlie elevated stroke volume and cardiac output of seawater-acclimated rainbow trout

Substantial increases in cardiac output (CO), stroke volume (SV), and gastrointestinal blood flow are essential for euryhaline rainbow trout (Oncorhyncus mykiss) osmoregulation in seawater. However, the underlying hemodynamic mechanisms responsible for these changes are unknown. By examining a range of circulatory and cardiac morphological variables of seawater- and freshwater-acclimated rainbow trout, the present study revealed a significantly higher central venous pressure (CVP) in seawater-acclimated trout (~0.09 vs. -0.02 kPa). This serves to increase cardiac end-diastolic volume in seawater and explains the elevations in SV (~0.41 vs. 0.27 ml/kg) and CO (~21.5 vs. 14.2 ml·min-1·kg-1) when compared with trout in freshwater. Furthermore, these hemodynamic modifications coincided with a significant increase in the proportion of compact myocardium, which may be necessary to compensate for the increased wall tension associated with a larger stroke volume. Following a temperature increase from 10 to 16.5°C, both acclimation groups exhibited similar increases in heart rate (Q10 of ~2), but SV tended to decrease in seawater-acclimated trout despite the fact that CVP was maintained in both groups. This resulted in CO of seawater- and freshwater-acclimated trout stabilizing at a similar level after warming (~26 ml·min-1·kg-1). The consistently higher CVP of seawater-acclimated trout suggests that factors other than compromised cardiac filling constrained the SV and CO of these individuals at high temperatures. The present study highlights, for the first time, the complex interacting effects of temperature and water salinity on cardiovascular responses in a euryhaline fish species.

Studying behavioural variation in salmonids from an ecological perspective: observations questions methodological considerations

Salmonid fish are an ecologically important and extensively studied group of fish which concern many interest groups in our society. The aim of this paper is to discuss and suggest solutions to the multifaceted problems associated with studying behavioural variation in salmonids, with focus on designing behavioural studies that are ecologically relevant. Many of the general problems and solutions discussed can be applied to other animals as well. First, the importance of asking clear questions when conceiving behavioural studies is addressed, using Tinbergen’s four questions and associated theories as stepping stones towards generating testable hypotheses about behavioural variation. We then address a range of methodological challenges encountered when attempting to study behavioural variation in salmonids and suggest solutions to overcome these problems. A range of approaches is discussed, from highly controllable laboratory experiments to monitoring studies of behaviour in the wild. The importance of combining lab- and field approaches to evaluate the ecological relevance of behavioural variation is highlighted. Finally, we suggest a general framework using a multi-faceted research approach to address questions about the behavioural ecology of salmonids (and other animals) so that knowledge can progress, and the ecological relevance of behavioural studies can be validated.

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.