Local thermal adaptation and local temperature regimes drive the performance of a parasitic helminth under climate change: The case of Marshallagia marshalli from wild ungulates.

Across a species' range, populations are exposed to their local thermal environments, which on an evolutionary scale, may cause adaptative differences among populations. Helminths often have broad geographic ranges and temperature-sensitive life stages but little is known about whether and how local thermal adaptation can influence their response to climate change. We studied the thermal responses of the free-living stages of Marshallagia marshalli, a parasitic nematode of wild ungulates, along a latitudinal gradient. We first determine its distribution in wild sheep species in North America. Then we cultured M. marshalli eggs from different locations at temperatures from 5 to 38°C. We fit performance curves based on the metabolic theory of ecology to determine whether development and mortality showed evidence of local thermal adaptation. We used parameter estimates in life-cycle-based host-parasite models to understand how local thermal responses may influence parasite performance under general and location-specific climate-change projections. We found that M. marshalli has a wide latitudinal and host range, infecting wild sheep species from New Mexico to Yukon. Increases in mortality and development time at higher temperatures were most evident for isolates from northern locations. Accounting for location-specific parasite parameters primarily influenced the magnitude of climate change parasite performance, while accounting for location-specific climates primarily influenced the phenology of parasite performance. Despite differences in development and mortality among M. marshalli populations, when using site-specific climate change projections, there was a similar magnitude of impact on the relative performance of M. marshalli among populations. Climate change is predicted to decrease the expected lifetime reproductive output of M. marshalli in all populations while delaying its seasonal peak by approximately 1 month. Our research suggests that accurate projections of the impacts of climate change on broadly distributed species need to consider local adaptations of organisms together with local temperature profiles and climate projections.

Behaviour is more important than thermal performance for an Arctic host-parasite system under climate change.

Climate change is affecting Arctic ecosystems, including parasites. Predicting outcomes for host-parasite systems is challenging due to the complexity of multi-species interactions and the numerous, interacting pathways by which climate change can alter dynamics. Increasing temperatures may lead to faster development of free-living parasite stages but also higher mortality. Interactions between behavioural plasticity of hosts and parasites will also influence transmission processes. We combined laboratory experiments and population modelling to understand the impacts of changing temperatures on barren-ground caribou (Rangifer tarandus) and their common helminth (Ostertagia gruehneri). We experimentally determined the thermal performance curves for mortality and development of free-living parasite stages and applied them in a spatial host-parasite model that also included behaviour of the parasite (propensity for arrested development in the host) and host (long-distance migration). Sensitivity analyses showed that thermal responses had less of an impact on simulated parasite burdens than expected, and the effect differed depending on parasite behaviour. The propensity for arrested development and host migration led to distinct spatio-temporal patterns in infection. These results emphasize the importance of considering behaviour-and behavioural plasticity-when projecting climate-change impacts on host-parasite systems.

Migratory hosts can maintain the high-dose/refuge effect in a structured host-parasite system: The case of sea lice and salmon.

Migration can reduce parasite burdens in migratory hosts, but it connects populations and can drive disease dynamics in domestic species. Farmed salmon are infested by sea louse parasites, often carried by migratory wild salmonids, resulting in a costly problem for industry and risk to wild populations when farms amplify louse numbers. Chemical treatment can control lice, but resistance has evolved in many salmon-farming regions. Resistance has, however, been slow to evolve in the north-east Pacific Ocean, where large wild-salmon populations harbour large sea louse populations. Using a mathematical model of host-macroparasite dynamics, we explored the roles of domestic, wild oceanic and connective migratory host populations in maintaining treatment susceptibility in associated sea lice. Our results show that a large wild salmon population, unexposed to direct infestation by lice from farms; high levels of on-farm treatment; and a healthy migratory host population are all critical to slowing or stopping the evolution of treatment resistance. Our results reproduce the "high-dose/refuge effect," from the agricultural literature, with the added requirement of a migratory host population to maintain treatment susceptibility. This work highlights the role that migratory hosts may play in shared wildlife/livestock disease, where evolution can occur in ecological time.

A unifying framework for the transient parasite dynamics of migratory hosts.

Migrations allow animals to track seasonal changes in resources, find mates, and avoid harsh climates, but these regular, long-distance movements also have implications for parasite dynamics and animal health. Migratory animals have been dubbed "superspreaders" of infection, but migration can also reduce parasite burdens within host populations via migratory escape from contaminated habitats and transmission hotspots, migratory recovery due to parasite mortality, and migratory culling of infected individuals. Here, we show that a single migratory host-macroparasite model can give rise to these different phenomena under different parametrizations, providing a unifying framework for a mechanistic understanding of the parasite dynamics of migratory animals. Importantly, our model includes the impact of parasite burden on host movement capability during migration, which can lead to "parasite-induced migratory stalling" due to a positive feedback between increasing parasite burdens and reduced movement. Our results provide general insight into the conditions leading to different health outcomes in migratory wildlife. Our approach lays the foundation for tactical models that can help understand, predict, and mitigate future changes of disease risk in migratory wildlife that may arise from shifting migratory patterns, loss of migratory behavior, or climate effects on parasite development, mortality, and transmission.

Correction to: Temperature-dependent development and freezing survival of protostrongylid nematodes of Arctic ungulates: implications for transmission.

Unfortunately, the original version of this article [1] contained an error.

Temperature-dependent development and freezing survival of protostrongylid nematodes of Arctic ungulates: implications for transmission.

BACKGROUND: Umingmakstrongylus pallikuukensis and Varestrongylus eleguneniensis are two potentially pathogenic lungworms of caribou and muskoxen in the Canadian Arctic. These parasites are currently undergoing northward range expansion at differential rates. It is hypothesized that their invasion and spread to the Canadian Arctic Archipelago are in part driven by climate warming. However, very little is known regarding their physiological ecology, limiting our ability to parameterize ecological models to test these hypotheses and make meaningful predictions. In this study, the developmental parameters of V. eleguneniensis inside a gastropod intermediate host were determined and freezing survival of U. pallikuukensis and V. eleguneniensis were compared. METHODS: Slug intermediate hosts, Deroceras laeve, were collected from their natural habitat and experimentally infected with first-stage larvae (L1) of V. eleguneniensis. Development of L1 to third-stage larvae (L3) in D. laeve was studied at constant temperature treatments from 8.5 to 24 °C. To determine freezing survival, freshly collected L1 of both parasite species were held in water at subzero temperatures from -10 to -80 °C, and the number of L1 surviving were counted at 2, 7, 30, 90 and 180 days. RESULTS: The lower threshold temperature (T0) below which the larvae of V. eleguneniensis did not develop into L3 was 9.54 °C and the degree-days required for development (DD) was 171.25. Both U. pallikuukensis and V. eleguneniensis showed remarkable freeze tolerance: more than 80% of L1 survived across all temperatures and durations. Larval survival decreased with freezing duration but did not differ between the two species. CONCLUSION: Both U. pallikuukensis and V. eleguneniensis have high freezing survival that allows them to survive severe Arctic winters. The higher T0 and DD of V. eleguneniensis compared to U. pallikuukensis may contribute to the comparatively slower range expansion of the former. Our study advances knowledge of Arctic parasitology and provides ecological and physiological data that can be useful for parameterizing ecological models.

Macroparasite dynamics of migratory host populations.

Spatial variability in host density is a key factor affecting disease dynamics of wildlife, and yet there are few spatially explicit models of host-macroparasite dynamics. This limits our understanding of parasitism in migratory hosts, whose densities change considerably in both space and time. In this paper, we develop a model for host-macroparasite dynamics that considers the directional movement of host populations and their associated parasites. We include spatiotemporal changes in the mean and variance in parasite burden per host, as well as parasite-mediated host mortality and parasite-mediated migratory ability. Reduced migratory ability with increasing parasitism results in heavily infested hosts halting their migration, and higher parasite burdens in stationary hosts than in moving hosts. Simulations reveal the potential for positive feedbacks between parasite-reduced migratory ability and increasing parasite burdens at infection hotspots, such as stopover sites, that may lead to parasite-induced migratory stalling. This framework could help understand how global change might influence wildlife disease via changes to migratory patterns and parasite demographic rates.

An asymmetric producer-scrounger game: body size and the social foraging behavior of coho salmon.

A tension between cooperation and conflict characterizes the behavioral dynamics of many social species. The foraging benefits of group living include increased efficiency and reduced need for vigilance, but social foraging can also encourage theft of captured prey from conspecifics. The payoffs of stealing prey from others (scrounging) versus capturing prey (producing) may depend not only on the frequency of each foraging strategy in the group but also on an individual's ability to steal. By observing the foraging behavior of juvenile coho salmon (Oncorhynchus kisutch), we found that, within a group, relatively smaller coho acted primarily as producers and took longer to handle prey, and were therefore more likely to be targeted by scroungers than relatively larger coho. Further, our observations suggest that the frequency of scrounging may be higher when groups contained individuals of different sizes. Based on these observations, we developed a model of phenotype-limited producer-scrounger dynamics, in which rates of stealing were structured by the relative size of producers and scroungers within the foraging group. Model simulations show that when the success of stealing is positively related to body size, relatively large predators should tend to be scroungers while smaller predators should be producers. Contrary to previous models, we also found that, under certain conditions, producer and scrounger strategies could coexist for both large and small phenotypes. Large scroungers tended to receive the highest payoff, suggesting that producer-scrounger dynamics may result in an uneven distribution of benefits among group members that-under the right conditions-could entrench social positions of dominance.

Sea-louse parasites on juvenile wild salmon in the Broughton Archipelago, British Columbia, Canada.

The global expansion of aquaculture has changed the structure of fish populations in coastal environments, with implications for disease dynamics. In Pacific Canada, farmed salmon act as reservoir hosts for parasites and pathogens, including sea lice (Lepeophtheirus salmonis and Caligus clemensi) that can transmit to migrating wild salmon. Assessing the impact of salmon farms on wild salmon requires regular monitoring of sea-louse infections on both farmed and wild fish. Since 2001, we have collected juvenile pink (Oncorhynchus gorbuscha) and chum (O. keta) salmon annually at three sites in the Broughton Archipelago in British Columbia, Canada, during the annual juvenile salmon migration from fresh water to the open ocean. From sampled fish, we recorded counts of parasitic copepodid-, chalimus-, and motile-stage sea lice. We report louse abundances as well as supplementary observations of fish size, development, and health.

Lessons from sea louse and salmon epidemiology.

Effective disease management can benefit from mathematical models that identify drivers of epidemiological change and guide decision-making. This is well illustrated in the host-parasite system of sea lice and salmon, which has been modelled extensively due to the economic costs associated with sea louse infections on salmon farms and the conservation concerns associated with sea louse infections on wild salmon. Consequently, a rich modelling literature devoted to sea louse and salmon epidemiology has been developed. We provide a synthesis of the mathematical and statistical models that have been used to study the epidemiology of sea lice and salmon. These studies span both conceptual and tactical models to quantify the effects of infections on host populations and communities, describe and predict patterns of transmission and dispersal, and guide evidence-based management of wild and farmed salmon. As aquaculture production continues to increase, advances made in modelling sea louse and salmon epidemiology should inform the sustainable management of marine resources.

Can reduced predation offset negative effects of sea louse parasites on chum salmon?

The impact of parasites on hosts is invariably negative when considered in isolation, but may be complex and unexpected in nature. For example, if parasites make hosts less desirable to predators then gains from reduced predation may offset direct costs of being parasitized. We explore these ideas in the context of sea louse infestations on salmon. In Pacific Canada, sea lice can spread from farmed salmon to migrating juvenile wild salmon. Low numbers of sea lice can cause mortality of juvenile pink and chum salmon. For pink salmon, this has resulted in reduced productivity of river populations exposed to salmon farming. However, for chum salmon, we did not find an effect of sea louse infestations on productivity, despite high statistical power. Motivated by this unexpected result, we used a mathematical model to show how a parasite-induced shift in predation pressure from chum salmon to pink salmon could offset negative direct impacts of sea lice on chum salmon. This shift in predation is proposed to occur because predators show an innate preference for pink salmon prey. This preference may be more easily expressed when sea lice compromise juvenile salmon hosts, making them easier to catch. Our results indicate how the ecological context of host-parasite interactions may dampen, or even reverse, the expected impact of parasites on host populations.

Cessation of a salmon decline with control of parasites.

The resilience of coastal social-ecological systems may depend on adaptive responses to aquaculture disease outbreaks that can threaten wild and farm fish. A nine-year study of parasitic sea lice (Lepeophtheirus salmonis) and pink salmon (Oncorhynchus gorbuscha) from Pacific Canada indicates that adaptive changes in parasite management on salmon farms have yielded positive conservation outcomes. After four years of sea lice epizootics and wild salmon population decline, parasiticide application on salmon farms was adapted to the timing of wild salmon migrations. Winter treatment of farm fish with parasiticides, prior to the out-migration of wild juvenile salmon, has reduced epizootics of wild salmon without significantly increasing the annual number of treatments. Levels of parasites on wild juvenile salmon significantly influence the growth rate of affected salmon populations, suggesting that these changes in management have had positive outcomes for wild salmon populations. These adaptive changes have not occurred through formal adaptive management, but rather, through multi-stakeholder processes arising from a contentious scientific and public debate. Despite the apparent success of parasite control on salmon farms in the study region, there remain concerns about the long-term sustainability of this approach because of the unknown ecological effects of parasticides and the potential for parasite resistance to chemical treatments.

Modeling parasite dynamics on farmed salmon for precautionary conservation management of wild salmon.

Conservation management of wild fish may include fish health management in sympatric populations of domesticated fish in aquaculture. We developed a mathematical model for the population dynamics of parasitic sea lice (Lepeophtheirus salmonis) on domesticated populations of Atlantic salmon (Salmo salar) in the Broughton Archipelago region of British Columbia. The model was fit to a seven-year dataset of monthly sea louse counts on farms in the area to estimate population growth rates in relation to abiotic factors (temperature and salinity), local host density (measured as cohort surface area), and the use of a parasiticide, emamectin benzoate, on farms. We then used the model to evaluate management scenarios in relation to policy guidelines that seek to keep motile louse abundance below an average three per farmed salmon during the March-June juvenile wild Pacific salmon (Oncorhynchus spp.) migration. Abiotic factors mediated the duration of effectiveness of parasiticide treatments, and results suggest treatment of farmed salmon conducted in January or early February minimized average louse abundance per farmed salmon during the juvenile wild salmon migration. Adapting the management of parasites on farmed salmon according to migrations of wild salmon may therefore provide a precautionary approach to conserving wild salmon populations in salmon farming regions.