Péter K. Molnár

Metabolic approaches to understanding climate change impacts on seasonal host-macroparasite dynamics

Climate change is expected to alter the dynamics of infectious diseases around the globe. Predictive models remain elusive due to the complexity of host-parasite systems and insufficient data describing how environmental conditions affect various system components. Here, we link host-macroparasite models with the Metabolic Theory of Ecology, providing a mechanistic framework that allows integrating multiple nonlinear environmental effects to estimate parasite fitness under novel conditions. The models allow determining the fundamental thermal niche of a parasite, and thus, whether climate change leads to range contraction or may permit a range expansion. Applying the models to seasonal environments, and using an arctic nematode with an endotherm host for illustration, we show that climate warming can split a continuous spring-to-fall transmission season into two separate transmission seasons with altered timings. Although the models are strategic and most suitable to evaluate broad-scale patterns of climate change impacts, close correspondence between model predictions and empirical data indicates model applicability also at the species level. As the application of Metabolic Theory considerably aids the a priori estimation of model parameters, even in data-sparse systems, we suggest that the presented approach could provide a framework for understanding and predicting climatic impacts for many host-parasite systems worldwide.

A walk on the tundra: Host–parasite interactions in an extreme environment

Climate change is occurring very rapidly in the Arctic, and the processes that have taken millions of years to evolve in this very extreme environment are now changing on timescales as short as decades. These changes are dramatic, subtle and non-linear. In this article, we discuss the evolving insights into host-parasite interactions for wild ungulate species, specifically, muskoxen and caribou, in the North American Arctic. These interactions occur in an environment that is characterized by extremes in temperature, high seasonality, and low host species abundance and diversity. We believe that lessons learned in this system can guide wildlife management and conservation throughout the Arctic, and can also be generalized to more broadly understand host-parasite interactions elsewhere. We specifically examine the impacts of climate change on host-parasite interactions and focus on: (I) the direct temperature effects on parasites; (II) the importance of considering the intricacies of host and parasite ecology for anticipating climate change impacts; and (III) the effect of shifting ecological barriers and corridors. Insights gained from studying the history and ecology of host-parasite systems in the Arctic will be central to understanding the role that climate change is playing in these more complex systems.

Climate change and Arctic parasites

Climate is changing rapidly in the Arctic. This has important implications for parasites of Arctic ungulates, and hence for the welfare of Arctic peoples who depend on caribou, reindeer, and muskoxen for food, income, and a focus for cultural activities. In this Opinion article we briefly review recent work on the development of predictive models for the impacts of climate change on helminth parasites and other pathogens of Arctic wildlife, in the hope that such models may eventually allow proactive mitigation and conservation strategies. We describe models that have been developed using the metabolic theory of ecology. The main strength of these models is that they can be easily parameterized using basic information about the physical size of the parasite. Initial results suggest they provide important new insights that are likely to generalize to a range of host-parasite systems.

Estimating Allee Dynamics before They Can Be Observed: Polar Bears as a Case Study

Allee effects are an important component in the population dynamics of numerous species. Accounting for these Allee effects in population viability analyses generally requires estimates of low-density population growth rates, but such data are unavailable for most species and particularly difficult to obtain for large mammals. Here, we present a mechanistic modeling framework that allows estimating the expected low-density growth rates under a mate-finding Allee effect before the Allee effect occurs or can be observed. The approach relies on representing the mechanisms causing the Allee effect in a process-based model, which can be parameterized and validated from data on the mechanisms rather than data on population growth. We illustrate the approach using polar bears (Ursus maritimus), and estimate their expected low-density growth by linking a mating dynamics model to a matrix projection model. The Allee threshold, defined as the population density below which growth becomes negative, is shown to depend on age-structure, sex ratio, and the life history parameters determining reproduction and survival. The Allee threshold is thus both density- and frequency-dependent. Sensitivity analyses of the Allee threshold show that different combinations of the parameters determining reproduction and survival can lead to differing Allee thresholds, even if these differing combinations imply the same stable-stage population growth rate. The approach further shows how mate-limitation can induce long transient dynamics, even in populations that eventually grow to carrying capacity. Applying the models to the overharvested low-density polar bear population of Viscount Melville Sound, Canada, shows that a mate-finding Allee effect is a plausible mechanism for slow recovery of this population. Our approach is generalizable to any mating system and life cycle, and could aid proactive management and conservation strategies, for example, by providing a priori estimates of minimum conservation targets for rare species or minimum eradication targets for pests and invasive species.

Empirical evidence that metabolic theory describes the temperature dependency of within-host parasite dynamics

The complexity of host–parasite interactions makes it difficult to predict how host–parasite systems will respond to climate change. In particular, host and parasite traits such as survival and virulence may have distinct temperature dependencies that must be integrated into models of disease dynamics. Using experimental data from Daphnia magna and a microsporidian parasite, we fitted a mechanistic model of the within-host parasite population dynamics. Model parameters comprising host aging and mortality, as well as parasite growth, virulence, and equilibrium abundance, were specified by relationships arising from the metabolic theory of ecology. The model effectively predicts host survival, parasite growth, and the cost of infection across temperature while using less than half the parameters compared to modeling temperatures discretely. Our results serve as a proof of concept that linking simple metabolic models with a mechanistic host–parasite framework can be used to predict temperature responses of parasite population dynamics at the within-host level.

Skewed temperature dependence affects range and abundance in a warming world

Population growth metrics such as R0 are usually asymmetric functions of temperature, with cold-skewed curves arising when the positive effects of a temperature increase outweigh the negative effects, and warm-skewed curves arising in the opposite case. Classically, cold-skewed curves are interpreted as more beneficial to a species under climate warming, because coldskewness implies increased population growth over a larger proportion of the species’ fundamental thermal niche than warm-skewness. However, inference based on the shape of the fitness curve alone, and without considering the synergistic effects of net reproduction, density, and dispersal may yield an incomplete understanding of climate change impacts. We formulate a moving-habitat integrodifference equation model to evaluate how fitness curve skewness affects species’ range size and abundance during climate warming. In contrast to classic interpretations, we find that climate warming adversely affects populations with cold-skewed fitness curves, positively affects populations with warm-skewed curves and has relatively little or mixed effects on populations with symmetric curves. Our results highlight the necessity of considering the synergistic effects of fitness curve skewness, density, and dispersal in climate change impact analyses, and that the common approach of mapping changes only in R0 may be misleading.

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.

Secondary forest is utilized by Great Curassows (Crax rubra) and Great Tinamous (Tinamus major) in the absence of hunting

ABSTRACT Deforestation and hunting are the leading human-driven disturbances causing population declines of the vulnerable Great Curassow (Crax rubra) and the near threatened Great Tinamou (Tinamus major). These threats typically co-occur, with synergistic effects. We investigated habitat use of Great Curassows and Great Tinamous in the Matapalo corridor of the Osa Peninsula, southwest Costa Rica, where they are not hunted, to understand whether disturbed habitats can be suitable for these species. We analyzed camera trap data from 56 locations and 5579 trapping days using occupancy modeling. We obtained 195 independent captures of Great Curassows at 33 of 56 locations (59%) and 429 independent captures of Great Tinamous at 37 of 56 locations (66%). Great Curassow occupancy did not vary with habitat type but was negatively influenced by distance from roads and by elevation; detection probability varied with habitat type. Great Tinamou occupancy probability was principally related to habitat type; primary, secondary and plantation forest areas all displayed high occupancy probabilities, but occupancy of agricultural land was low. Our work suggests that secondary-growth forests can offer valuable complementary habitat to assist in the recovery of these declining species, at least when hunting is controlled and intact forests are nearby.