Ontogenetic Change in Behavioral Responses to Structural Enrichment From Fry to Parr in Juvenile Atlantic Salmon (Salmo salar L.).

Enrichment is widely used as a tool for studying how changes in environment affect animal behavior. Here, we report an experimental study investigating if behaviors shaped by stimuli from environmental enrichment depending on the stage animals are exposed to enrichment. We used juvenile Atlantic salmon (Salmo salar) in their first autumn. This is a species commonly reared for conservation purposes. Previous work has shown that environmental enrichment had no effect on long-term survival when the fry stage (smaller than 70 mm) was released, but that if late parr stages (larger than 70 mm) are released, enrichment is reported to have a positive effect on smolt migration survival. Here, we explored the effect of enrichment at two different stages of development. Both stages were reared and treated for 7 weeks (fry at 11-18 weeks and parr at 24-31 weeks after hatching) before tested for behavior. Responses known to be associated with exploratory behavior, activity, and stress coping were quantified by testing 18-week-old fry and 31-week-old parr in a six-chamber maze on 7 successive days after rearing in structurally enriched (plastic plants and tubes) or plain impoverished rearing environments. The data show that Atlantic salmon are sensitive to stimuli from structural enrichment when they are parr, but not when in the fry stage. Parr deprived of enrichment (control treatment) were reluctant to start exploring the maze, and when they did, they spent a longer time frozen than enriched parr, suggesting that deprivation of enrichment at this life can be stressful. Our data suggest that structural enrichment could have the potential to improve welfare for salmonids in captivity and for survival of released juvenile salmon if structural enrichment is provided at the parr stage and the fish reared for conservation are released at the parr stage.

Duration of the parasitic phase determines subsequent performance in juvenile freshwater pearl mussels (Margaritifera margaritifera).

Host-parasite systems have been useful in understanding coevolutionary patterns in sympatric species. Based on the exceptional interaction of the long-lived and highly host-specific freshwater pearl mussel (FPM; Margaritifera margaritifera) with its much shorter-lived host fish (Salmo trutta or Salmo salar), we tested the hypotheses that a longer duration of the parasitic phase increases fitness-related performance of mussels in their subsequent post parasitic phase, and that temperature is the main factor governing the duration of the parasitic phase. We collected juvenile mussels from naturally and artificially infested fish from eight rivers in Norway. Excysted juvenile mussels were maintained separately for each collection day, under similar temperature and food regimes, for up to 56 days. We recorded size at excystment, post excystment growth, and survival as indicators of juvenile fitness in relation to the duration of the parasitic phase. We also recorded the daily average temperatures for the entire excystment period. We observed strong positive relationships between the length of the parasitic phase and the post parasitic growth rate, size at excystment and post parasitic survival. Temperature was identified as an important factor governing excystment, with higher temperatures decreasing the duration of the parasitic phase. Our results indicate that juvenile mussels with the longest parasitic phase have better resources (larger size and better growth rate) to start their benthic developmental phase and therefore to survive their first winter. Consequently, the parasitic phase is crucial in determining subsequent survival. The temperature dependence of this interaction suggests that climate change may affect the sensitive relationship between endangered FPMs and their fish hosts.

An Enriched Environment Promotes Shelter-Seeking Behaviour and Survival of Hatchery-Produced Juvenile European Lobster (Homarus gammarus).

The high loss of newly released hatchery-reared European lobster (Homarus gammarus) juveniles for stock enhancement is believed to be the result of maladaptive anti-predator behaviour connected to deprived stimuli in the hatchery environment. Our objective was to learn if an enriched hatchery environment enhances shelter-seeking behaviour and survival. In the "naïve" treatment, the juveniles were raised in single compartments without substrate and shelter whereas juveniles in the "exposed" treatment experienced substrate, shelter and interactions with conspecifics. Three experiments with increasing complexity were conducted. Few differences in shelter-seeking behaviour were found between treatments when one naïve or one exposed juvenile were observed alone. When observing interactions between one naïve and one exposed juvenile competing for shelter, naïve juveniles more often initiated the first aggressive encounter. The third experiment was set up to simulate a release for stock enhancement. Naïve and exposed juveniles were introduced to a semi-natural environment including substrate, a limited number of shelters and interactions with conspecifics. Shelter occupancy was recorded three times during a period of 35 days. Exposed juveniles occupied more shelters, grew larger and had higher survival compared with naïve juveniles. Our results demonstrate that experience of environmental complexity and social interactions increase shelter-seeking ability and survival in hatchery reared lobster juveniles.

When to Reproduce? A New Answer to an Old Question.

We present a life-history model based on the assumptions that juvenile survival follows a negative exponential function and that fecundity gain increases linearly with time to maturity. This model predicts that the optimal fitness is achieved when survival at maturity is 0.368 (e(-1)). Survival at the time of maturity is therefore an invariant. We tested this prediction by using published data from infection experiments with mammalian nematodes, where both the initial number of juveniles colonizing a habitat (host) and the numbers surviving at the time of maturation were known. We found that the mean survival at maturity, both across and within species, was remarkably close to our predicted mean. As a control, we also looked at studies where the parasite species was adapted to a host species other than the one used in the reported experiment. In these experiments the mean survival at maturity differed from what our model predicted. Maturation at a fixed survival probability therefore appears as an adaptive trait evolved in a predictable environment, in this case, a host species. Our result further suggests that measures designed to increase juvenile parasite mortality, such as drugs or vaccines, will select for faster developmental rates.

A characterization of the ZFL cell line and primary hepatocytes as in vitro liver cell models for the zebrafish (Danio rerio).

The zebrafish (Danio rerio) is a widely used model species in biomedical research. The ZFL cell line, established from zebrafish liver, and freshly isolated primary hepatocytes from zebrafish have been used in several toxicological studies. However, no previous report has compared and characterized these two systems at the level of gene expression. The aim of this study was to evaluate the ZFL cell line in comparison to primary hepatocytes as in vitro models for studying effects of environmental contaminants in zebrafish liver. Using quantitative real-time PCR, the basal level and transcriptional induction potential of key genes involved in toxic responses in the ZFL cell line, primary hepatocytes and whole liver from zebrafish were compared. The study showed that the ZFL cells have lower levels of mRNA of most selected genes compared to zebrafish liver. The induced gene transcription following exposure to ligand was much lower in ZFL cells compared to zebrafish primary hepatocytes at the doses tested. Importantly, oestrogen receptor and vitellogenin genes showed low basal transcription and no induction response in the ZFL cell line. In conclusion, it appears that primary hepatocytes are well suited for studying environmental contaminants including xenoestrogens, but may show large sex-dependent differences in gene transcription. The ZFL cell line shows potential in toxicological studies involving the aryl hydrocarbon receptor pathway. However, low potential for transcriptional induction of genes in general should be expected, especially notable when studying estrogenic responses.

Environmental enrichment promotes neural plasticity and cognitive ability in fish.

Different kinds of experience during early life can play a significant role in the development of an animal's behavioural phenotype. In natural contexts, this influences behaviours from anti-predator responses to navigation abilities. By contrast, for animals reared in captive environments, the homogeneous nature of their experience tends to reduce behavioural flexibility. Studies with cage-reared rodents indicate that captivity often compromises neural development and neural plasticity. Such neural and behavioural deficits can be problematic if captive-bred animals are being reared with the intention of releasing them as part of a conservation strategy. Over the last decade, there has been growing interest in the use of environmental enrichment to promote behavioural flexibility in animals that are bred for release. Here, we describe the positive effects of environmental enrichment on neural plasticity and cognition in juvenile Atlantic salmon (Salmo salar). Exposing fish to enriched conditions upregulated the forebrain expression of NeuroD1 mRNA and improved learning ability assessed in a spatial task. The addition of enrichment to the captive environment thus promotes neural and behavioural changes that are likely to promote behavioural flexibility and improve post-release survival.

Who benefits from reduced reproduction in parasitized hosts? An experimental test using the Pasteuria ramosa-Daphnia magna system.

We investigated whether parasites or hosts benefit from reduced reproduction in infected hosts. When parasites castrate their hosts, the regain of host reproduction is necessary for castration to be a host adaptation. When infecting Daphnia magna with Pasteuria ramosa, in a lake water based medium, 49 2% of the castrated females regained reproduction. We investigated the relationship between castration level, and parasite and host fitness proxies to determine the adaptive value of host castration. Hosts which regained reproduction contained less spores and had a higher lifetime reproduction than permanently castrated hosts. We also found a negative correlation between parasite and host lifetime reproduction. For hosts which regained reproduction we found no optimal level of castration associated with lifetime reproduction. These results support the view that host castration only is adaptive to the parasite in this system. In addition, we suggest that permanent castration might not be the norm under natural conditions in this system. Finally, we argue that a reduction in host reproduction is more likely to evolve as a property favouring parasites rather than hosts. To our knowledge this is the only experimental study to investigate the adaptive value of reduced host reproduction when castrated hosts can regain reproduction.

Empirical support for optimal virulence in a castrating parasite.

The trade-off hypothesis for the evolution of virulence predicts that parasite transmission stage production and host exploitation are balanced such that lifetime transmission success (LTS) is maximised. However, the experimental evidence for this prediction is weak, mainly because LTS, which indicates parasite fitness, has been difficult to measure. For castrating parasites, this simple model has been modified to take into account that parasites convert host reproductive resources into transmission stages. Parasites that kill the host too early will hardly benefit from these resources, while postponing the killing of the host results in diminished returns. As predicted from optimality models, a parasite inducing castration should therefore castrate early, but show intermediate levels of virulence, where virulence is measured as time to host killing. We studied virulence in an experimental system where a bacterial parasite castrates its host and produces spores that are not released until after host death. This permits estimating the LTS of the parasite, which can then be related to its virulence. We exposed replicate individual Daphnia magna (Crustacea) of one host clone to the same amount of bacterial spores and followed individuals until their death. We found that the parasite shows strong variation in the time to kill its host and that transmission stage production peaks at an intermediate level of virulence. A further experiment tested for the genetic basis of variation in virulence by comparing survival curves of daphniids infected with parasite spores obtained from early killing versus late killing infections. Hosts infected with early killer spores had a significantly higher death rate as compared to those infected with late killers, indicating that variation in time to death was at least in part caused by genetic differences among parasites. We speculate that the clear peak in lifetime reproductive success at intermediate killing times may be caused by the exceptionally strong physiological trade-off between host and parasite reproduction. This is the first experimental study to demonstrate that the production of propagules is highest at intermediate levels of virulence and that parasite genetic variability is available to drive the evolution of virulence in this system.

Vector-borne parasites decrease host mobility: a field test of freeze or flee behaviour of willow ptarmigan.

Transmission mode has been suggested to be a strong predictor of virulence. According to theory, the transmission of vector-borne parasites should be less dependent on host mobility than directly transmitted parasites. This could select for increased exploitation of host resources in parasites transmitted by vectors, which may be manifested as higher virulence. Here, we test the prediction that there is an association between transmission mode and the effect on host mobility by comparing parasite infection levels and mobility in willow ptarmigan (Lagopus lagopus L.). We examined the endoparasite infracommunities of individual hosts to obtain annual, quantitative data on four vector-transmitted species (Leucocytozoon lovati, Trypanosoma avium, Haemoproteus mansoni and microfilaria), two directly transmitted species (Trichostrongylus tenuis and Eimeria sp.) and two species with indirect life cycles (Hymenolepis microps and Parionella urogalli). We then used observed variations in freeze-or-flee responses of individual willow ptarmigan to assess whether parasite intensities were related to scored freezing responses. From a field data set covering a period of 9 years from a single area, we found that stronger freezing responses were associated with higher intensities of vector-borne parasites, especially with higher intensities of the haemosporidian L. lovati. Freezing responses were not associated with parasites transmitted in other ways. Thus, high intensities of vector-borne parasites tended to reduce host movements, while parasites with other transmission modes did not.

Variation in phenoloxidase activity and its relation to parasite resistance within and between populations of Daphnia magna.

Estimates of phenoloxidase (PO) activity have been suggested as a useful indicator of immunocompetence in arthropods, with the idea that high PO activity would indicate high immunocompetence against parasites and pathogens. Here, we test for variation in PO activity among clones of the planktonic crustacean Daphnia magna and its covariation with susceptibility to infections from four different microparasite species (one bacterium and three microsporidia). Strong clonal variation in PO activity was found within and among populations of D. magna, with 45.6% of the total variation being explained by the clone effect. Quantitative measures of parasite success in infection correlated negatively with PO activity when tested across four host populations. However, these correlations disappeared when the data were corrected for population effects. We conclude that PO activity is not a useful measure of resistance to parasites or of immunocompetence within populations of D. magna. We further tested whether D. magna females that are wounded to induce PO activity are more resistant to infections with the bacterium Pasteuria ramosa than non-wounded controls. We found neither a difference in susceptibility nor a difference in disease progression between the induced group and the control group. These results do not question the function of the PO system in arthropod immune response, but rather suggest that immunocompetence cannot be assessed by considering PO activity alone. Immune response is likely to be a multifactorial trait with various host and parasite characteristics playing important roles in its expression.

Disease dynamics: all caused by males?

Some host individuals tend to acquire parasites at a much faster rate than do others--a consequence of heterogeneities in susceptibility and/or exposure. This is termed 'overdispersion' and, as for many other statistical phenomena, the degree of overdispersion often conforms to a 20/80 rule, where 20% of the host population is responsible for approximately 80% of the parasite transmission. But which are the hosts driving so much of the dynamics of an infectious disease? If host individuals at the tail of the frequency distribution can be identified by some common label, controlling parasitic diseases would be much easier. In two recent papers, Perkins et al. and Ferrari et al. have shown that male hosts are much more important than female hosts in the transmission of parasites.