Effects of the invasive swim bladder parasite Anguillicola crassus on health and condition indicators in the European eel.

Parasites negatively affect biological processes within their hosts, which may alter for example health, growth, and reproductive ability. Non-native invasive parasites, in particular, may have large effects on the endemic hosts, given that the hosts lack evolved specific defences against such parasites. The swim bladder nematode Anguillicola crassus, an invasive parasite originating from Asia, is found in the European eel (Anguilla anguilla, L. 1758), since the 1980s. We investigated whether A. crassus affected several indicators related to health of the European eel (spleen- and liver size, body fat content and relative condition). Our results indicate that during the continental residency of the eels, infection by A. crassus had no major negative impacts on the investigated health indicators at the generally low infection intensities present in this study (median 2-3 visible parasites). Given that many of the adult eels were found to have swim bladder damage, concerns about their spawning migration through deeper oceanic environments can still be raised. To allow further investigations, we suggest that quantification of swim bladder damage should be implemented in eel-monitoring programs. Compared to other parasite pressure parameters, swim bladder damage provides additional information about past infections and future problems.

Social isolation affects intra-specific interaction behaviour and reduces the size of the cerebellar brain region in juvenile Atlantic salmon Salmo salar.

The social environment can affect the development of behavioural phenotypes in fish, and it is important to understand such effects when rearing fish in artificial environments. Here, the authors test the effects of spatial isolation on social interaction propensity and brain development in hatchery-reared Atlantic salmon Salmo salar L. Salmon reared in isolation generally stayed further away from a conspecific in a standardized intruder test than conspecifics reared together in groups. Isolated salmon also tended to be more active in an intruder test, albeit non-significantly so, but this pattern was not detected in open-field tests without an intruding conspecific. The cerebellar brain region was relatively smaller in isolated salmon, suggesting that the brain was developing differently in these fish. Therefore, some features of the behavioural and neural phenotype are affected by rearing in isolation. These effects should be considered when rearing salmon, particularly for experimental purposes as it may affect results of laboratory studies on behavioural expression and brain size.

Fast life-histories are associated with larger brain size in killifishes.

The high energetic demands associated with the vertebrate brain are proposed to result in a trade-off between the pace of life-history and relative brain size. However, because both life-history and brain size also have a strong relationship with body size, any associations between the pace of life-history and relative brain size may be confounded by coevolution with body size. Studies on systems where contrasts in the pace of life-history occur without concordant contrasts in body size could therefore add to our understanding of the potential coevolution between relative brain size and life-history. Using one such system - 21 species of killifish - we employed a common garden design across two ontogenetic stages to investigate the association between relative brain size and the pace of life-history. Contrary to predictions, we found that relative brain size was larger in adult fast-living killifishes, compared to slow-living species. Although we found no differences in relative brain size between juvenile killifishes. Our results suggest that fast- and slow-living killifishes do not exhibit the predicted trade-off between brain size and life-history. Instead, fast and slow-living killifishes could differ in the ontogenetic timing of somatic versus neural growth or inhabit environments that differ considerably in cognitive demands.

Variation in developmental rates is not linked to environmental unpredictability in annual killifishes.

Comparative evidence suggests that adaptive plasticity may evolve as a response to predictable environmental variation. However, less attention has been placed on unpredictable environmental variation, which is considered to affect evolutionary trajectories by increasing phenotypic variation (or bet hedging). Here, we examine the occurrence of bet hedging in egg developmental rates in seven species of annual killifish that originate from a gradient of variation in precipitation rates, under three treatment incubation temperatures (21, 23, and 25°C). In the wild, these species survive regular and seasonal habitat desiccation, as dormant eggs buried in the soil. At the onset of the rainy season, embryos must be sufficiently developed in order to hatch and complete their life cycle. We found substantial differences among species in both the mean and variation of egg development rates, as well as species-specific plastic responses to incubation temperature. Yet, there was no clear relationship between variation in egg development time and variation in precipitation rate (environmental predictability). The exact cause of these differences therefore remains enigmatic, possibly depending on differences in other natural environmental conditions in addition to precipitation predictability. Hence, if species-specific variances are adaptive, the relationship between development and variation in precipitation is complex and does not diverge in accordance with simple linear relationships.

Thermal performance under constant temperatures can accurately predict insect development times across naturally variable microclimates.

External conditions can drive biological rates in ectotherms by directly influencing body temperatures. While estimating the temperature dependence of performance traits such as growth and development rate is feasible under controlled laboratory settings, predictions in nature are difficult. One major challenge lies in translating performance under constant conditions to fluctuating environments. Using the butterfly Pieris napi as model system, we show that development rate, an important fitness trait, can be accurately predicted in the field using models parameterized under constant laboratory temperatures. Additionally, using a factorial design, we show that accurate predictions can be made across microhabitats but critically hinge on adequate consideration of non-linearity in reaction norms, spatial heterogeneity in microclimate and temporal variation in temperature. Our empirical results are also supported by a comparison of published and simulated data. Conclusively, our combined results suggest that, discounting direct effects of temperature, insect development rates are generally unaffected by thermal fluctuations.

Disentangling the nonlinear effects of habitat complexity on functional responses.

Structural complexity of habitats modifies trophic interactions by providing refuges and altering predator and prey behaviour. Nonlinear effects on trophic interaction strengths driven by these mechanisms may alter food web dynamics and community structure in response to habitat modifications. However, changes in functional response, the relationship between prey density and feeding rate, along habitat complexity (HC) gradients are little understood. We quantified functional responses along a HC gradient from an entirely unstructured to highly structured habitat in a freshwater system, using dragonfly larvae (Aeshna cyanea) preying on Chaoborus obscuripes larvae. To disentangle mechanisms by which changes in HC affect functional responses, we used two different approaches-a population-level and a behavioural experiment-applied an information theoretic approach to identify plausible links between HC and functional response parameters, and compared our results to previous studies. Functional response shape did not change, but we found strong evidence for nonlinear dependence of attack rate and handling time on HC in our study. Combined results from both experiments imply that attack rate increased stepwise between the unstructured and structured habitats in line with the threshold hypothesis, because the predators gained better access to the prey. Handling time was lowest at an intermediate HC level in the population-level experiment while the direct estimate of handling time did not vary with HC in the behavioural experiment. These differences point towards HC-driven changes in foraging activity and other predator and prey behaviour. Most previous studies reported stepwise decrease in attack rate in line with the threshold hypothesis or no change with increasing HC. Moreover, changes in the handling time parameter with HC appear to be relatively common but not conforming to the threshold hypothesis. Overall, increased HC appears to, respectively, weaken and strengthen trophic links in 2D and 3D predator-prey interactions. We conclude that detailed understanding of HC effects on food webs requires complementary experimental approaches across HC gradients that consider predator foraging strategies and predator and prey behaviour. Such studies can also help guide conservation efforts as addition of structural elements is frequently used for restoration of degraded aquatic habitats.

Mapping the distribution of scale-rayed wrasse Acantholabrus palloni in Swedish Skagerrak using angling records.

In this paper, we map the distribution of scale-rayed wrasse Acantholabrus palloni in eastern Skagerrak based on a combination of verified and personally communicated angling records. Long thought to be occasional vagrants outside its known range in the eastern Atlantic Ocean and Mediterranean Sea, we ask if this rare and understudied labrid has expanded its range and become established in Swedish waters. A recent surge in verified angling records in the Swedish Anglers Association's specimen database Storfiskregistret provides information to suggest that this species should no longer be considered an occasional guest, but rather a species established in the Swedish parts of Skagerrak. These records are supported by additional personal communications with anglers. The species is currently well spread geographically along the Swedish Skagerrak coast, with many locations providing repeated captures of adult fish over multiple years. The typical Swedish catch sites are rocky reefs located between the general 40- and 80-m depth curves, likely influenced by currents bringing higher-salinity water from the North Sea. The present study show that angling records can provide an important, but underutilized, resource for mapping the distribution of data-deficient fish species.

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.

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.

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.

State-dependent behavior and alternative behavioral strategies in brown trout (Salmo trutta L.) fry.

ABSTRACT: Animals generally adjust their behavior in response to bodily state (e.g., size and energy reserves) to optimize energy intake in relation to mortality risk, weighing predation probability against the risk of starvation. Here, we investigated whether brown trout Salmo trutta adjust their behavior in relation to energetic status and body size during a major early-life selection bottleneck, when fast growth is important. Over two consecutive time periods (P1 and P2; 12 and 23 days, respectively), food availability was manipulated, using four different combinations of high (H) and low (L) rations (i.e., HH, HL, LH, and LL; first and second letter denoting ration during P1 and P2, respectively). Social effects were excluded through individual isolation. Following the treatment periods, fish in the HL treatment were on average 15-21 % more active than the other groups in a forced open-field test, but large within-treatment variation provided only weak statistical support for this effect. Furthermore, fish on L-ration during P2 tended to be more actively aggressive towards their mirror image than fish on H-ration. Body size was related to behavioral expression, with larger fish being more active and aggressive. Swimming activity and active aggression were positively correlated, forming a behavioral syndrome in the studied population. Based on these behavioral traits, we could also distinguish two behavioral clusters: one consisting of more active and aggressive individuals and the other consisting of less active and aggressive individuals. This indicates that brown trout fry adopt distinct behavioral strategies early in life. SIGNIFICANCE STATEMENT: This paper provides information on the state-dependence of behavior in animals, in particular young brown trout. On the one hand, our data suggest a weak energetic state feedback where activity and aggression is increased as a response to short term food restriction. This suggests a limited scope for behavioral alterations in the face of starvation. On the other hand, body size is linked to higher activity and aggression, likely as a positive feedback between size and dominance. The experiment was carried out during the main population survival bottleneck, and the results indicate that growth is important during this stage, as 1) behavioral compensation to increase growth is limited, and 2) growth likely increases the competitive ability. However, our data also suggests that the population separates into two clusters, based on combined scores of activity and aggression (which are positively linked within individuals). Thus, apart from an active and aggressive strategy, there seems to be another more passive behavioral strategy.

Telomere dynamics in wild brown trout: effects of compensatory growth and early growth investment.

After a period of food deprivation, animals often respond with a period of faster than normal growth. Such responses have been suggested to result in decreased chromosomal maintenance, which in turn may affect the future fitness of an individual. Here, we present a field experiment in which a food deprivation period of 24 days was enforced on fish from a natural population of juvenile brown trout (Salmo trutta) at the start of the high-growth season in spring. The growth of the food-deprived fish and a non-deprived control group was then monitored in the wild during 1 year. Fin tissue samples were taken at the start of the experiment and 1 year after food deprivation to monitor the telomere dynamics, using reduced telomere length as an indicator of maintenance cost. The food-deprived fish showed partial compensatory growth in both mass and length relative to the control group. However, we found no treatment effects on telomere dynamics, suggesting that growth-compensating brown trout juveniles are able to maintain their telomeres during their second year in the stream. However, body size at the start of the experiment, reflecting growth rate during their first year of life, was negatively correlated with change in telomere length over the following year. This result raises the possibility that rapid growth early in life induces delayed costs in cellular maintenance.

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.

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 ghrelin's 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.