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.

Life history shifts in an exploited African fish following invasion by a castrating parasite.

Evolutionary theory predicts that infection by a parasite that reduces future host survival or fecundity should select for increased investment in current reproduction. In this study, we use the cestode Ligula intestinalis and its intermediate fish host Engraulicypris sardella in Wissman Bay, Lake Nyasa (Tanzania), as a model system. Using data about infection of E. sardella fish hosts by L. intestinalis collected for a period of 10 years, we explored whether parasite infection affects the fecundity of the fish host E. sardella, and whether host reproductive investment has increased at the expense of somatic growth. We found that L. intestinalis had a strong negative effect on the fecundity of its intermediate fish host. For the noninfected fish, we observed an increase in relative gonadal weight at maturity over the study period, while size at maturity decreased. These findings suggest that the life history of E. sardella has been shifting toward earlier reproduction. Further studies are warranted to assess whether these changes reflect plastic or evolutionary responses. We also discuss the interaction between parasite and fishery-mediated selection as a possible explanation for the decline of E. sardella stock in the lake.

The tapeworm Ligula intestinalis alters the behavior of the fish intermediate host Engraulicypris sardella, but only after it has become infective to the final host.

Ligula intestinalis is a tapeworm using copepods and cyprinid fish as intermediate hosts and fish-eating birds as final hosts. Since some parasites can increase their own fitness by manipulating the behavior of the intermediate host, we explored if this parasite affected predator avoidance, swimming activity and depth preference of the fish intermediate host, Engraulicypris sardella. We found that when L. intestinalis had reached a developmental stage that is able to establish in the bird host, it had a significant impact on E. sardella behavior, while the tapeworm that was not fully developed had little effect and fish hosts showed a behavior more similar to uninfected fish. These results are discussed with respect to two different processes: the manipulation hypothesis and the energy drain hypothesis.

Invest more and die faster: The life history of a parasite on intensive farms.

Organisms are expected to respond to alterations in their survival by evolutionary changes in their life history traits. As agriculture and aquaculture have become increasingly intensive in the past decades, there has been growing interest in their evolutionary effects on the life histories of agri- and aquacultural pests, parasites, and pathogens. In this study, we used salmon lice (Lepeophtheirus salmonis) to explore how modern farming might have affected life history evolution in parasites. We infected salmon hosts with lice from either farmed or unfarmed locations, and monitored life history traits of those parasites in laboratory conditions. Our results show that compared to salmon lice from areas unaffected by salmon farming, those from farmed areas produced more eggs in their first clutch, and less eggs later on; they achieved higher infestation intensities in early adulthood, but suffered higher adult mortality. These results suggest that salmon lice on farms may have been selected for increased investment in early reproduction, at the expense of later fecundity and survival. This call for further empirical studies of the extent to which farming practices may alter the virulence of agricultural parasites.

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.

Intensive Farming: Evolutionary Implications for Parasites and Pathogens.

An increasing number of scientists have recently raised concerns about the threat posed by human intervention on the evolution of parasites and disease agents. New parasites (including pathogens) keep emerging and parasites which previously were considered to be 'under control' are re-emerging, sometimes in highly virulent forms. This re-emergence may be parasite evolution, driven by human activity, including ecological changes related to modern agricultural practices. Intensive farming creates conditions for parasite growth and transmission drastically different from what parasites experience in wild host populations and may therefore alter selection on various traits, such as life-history traits and virulence. Although recent epidemic outbreaks highlight the risks associated with intensive farming practices, most work has focused on reducing the short-term economic losses imposed by parasites, such as application of chemotherapy. Most of the research on parasite evolution has been conducted using laboratory model systems, often unrelated to economically important systems. Here, we review the possible evolutionary consequences of intensive farming by relating current knowledge of the evolution of parasite life-history and virulence with specific conditions experienced by parasites on farms. We show that intensive farming practices are likely to select for fast-growing, early-transmitted, and hence probably more virulent parasites. As an illustration, we consider the case of the fish farming industry, a branch of intensive farming which has dramatically expanded recently and present evidence that supports the idea that intensive farming conditions increase parasite virulence. We suggest that more studies should focus on the impact of intensive farming on parasite evolution in order to build currently lacking, but necessary bridges between academia and decision-makers.

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.

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.

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.

Standard sampling techniques underestimate prevalence of avian hematozoa in willow ptarmigan (Lagopus lagopus).

A total of 68 willow ptarmigan (Lagopus lagopus L.) was collected during September 1995 from two localities in Troms County, northern Norway. Thin blood smears were prepared and examined for blood parasites. Of the 68 willow ptarmigan examined, 94% harbored one or more species of hematozoa. There were four (6%), 44 (65%), 16 (24%), and four (6%) birds infected by zero, one, two, and three species of parasites, respectively. Prevalences at the coastal locality, Kattfjord (n = 43), were Leucocytozoon lovati 86%, Trypanosoma avium (26%), and microfilariae (30%). At the inland locality, Iselvdalen (n = 25), prevalences were L. lovati 96%, T. avium 12%, and microfilariae 0%. We also searched connective tissues for the filaroid nematode Splendidofilaria papillocerca; in Kattfjord this parasite only occurred in adult hosts where prevalence was 94%, but the parasite was not found in Iselvdalen. To estimate the efficiency of parasite detection by standard blood sampling techniques, we sampled peripheral blood from the brachial wing vein and blood from the pulmonary system from willow ptarmigan. Sampling peripheral blood from the brachial vein led to underestimates of the prevalence of microfilariae. There was no significant difference between L. lovati and T. avium prevalence in blood collected from the brachial vein or deep circulation. Age of host had a strong impact on prevalence, especially for S. papillocerca and microfilariae.

Density-dependent effects in a parasitic nematode, Elaphostrongylus rangiferi, in the snnail intermediate host.

Density-dependent effects in Elaphostrongylus rangiferi, a parasitic nematode in the CNS and muscular system of reindeer, were studied in a laboratory population of the snail intermediate host, Arianta arbustorum. The rates in parasite growth, development and mortality were all affected by parasite density. The effects on growth and development were, however, much more marked, than the effect on mortality.All density-dependent rates were intensified by decreasing snail size, and by snail starvation. The snail host showed marked tissue reactions against infection, and the intensity of these reactions increased with increasing parasite density. The mechanism behind the observed density-dependent rates is discussed, and is tentatively concluded to be competition for nutritive substances in the host tissue.The importance of a density-dependent developmental rate in natural populations of this parasite is discussed, and it is hypothesized that this effect may counteract the strong temperature-dependent developmental rate of E. rangiferi In a more general context it is pointed out that density-dependent developmental rates, although common amongst animal populations, has been neglected in models of population dynamics. Developmental rates are usually represented by a constant time lag in such models, but should be treated as a density-dependent variable.