Emily J. Jenkins

Global warming is changing the dynamics of Arctic host–parasite systems

Global climate change is altering the ecology of infectious agents and driving the emergence of disease in people, domestic animals, and wildlife. We present a novel, empirically based, predictive model for the impact of climate warming on development rates and availability of an important parasitic nematode of muskoxen in the Canadian Arctic, a region that is particularly vulnerable to climate change. Using this model, we show that warming in the Arctic may have already radically altered the transmission dynamics of this parasite, escalating infection pressure for muskoxen, and that this trend is expected to continue. This work establishes a foundation for understanding responses to climate change of other host–parasite systems, in the Arctic and globally.

The Arctic as a model for anticipating, preventing, and mitigating climate change impacts on host-parasite interactions.

Climate change is influencing the structure and function of natural ecosystems around the world, including host-parasite interactions and disease emergence. Understanding the influence of climate change on infectious disease at temperate and tropical latitudes can be challenging because of numerous complicating biological, social, and political factors. Arctic and Subarctic regions may be particularly good models for unraveling the impacts of climate change on parasite ecology because they are relatively simple systems with low biological diversity and few other complicating anthropogenic factors. We examine some changing dynamics of host-parasite interactions at high latitudes and use these to illustrate a framework for approaching understanding, preventing, and mitigating climate change impacts on infectious disease, including zoonoses, in wildlife.

The impact of globalisation on the distribution of Echinococcus multilocularis.

In the past three decades, Echinococcus multilocularis, the cause of human alveolar echinococcosis, has been reported in several new countries both in definitive hosts (canids) as well as in people. Unless treated, infection with this cestode in people is fatal. In previously endemic countries throughout the Northern Hemisphere, geographic ranges and human and animal prevalence levels seem to be increasing. Anthropogenic influences, including increased globalisation of animals and animal products, and altered human/animal interfaces are thought to play a vital role in the global emergence of this pathogenic cestode. Molecular epidemiological techniques are a useful tool for detecting and tracing introductions, and differentiating these from range expansions.

Tradition and transition: Parasitic zoonoses of people and animals in Alaska, northern Canada, and Greenland

Zoonotic parasites are important causes of endemic and emerging human disease in northern North America and Greenland (the North), where prevalence of some parasites is higher than in the general North American population. The North today is in transition, facing increased resource extraction, globalisation of trade and travel, and rapid and accelerating environmental change. This comprehensive review addresses the diversity, distribution, ecology, epidemiology, and significance of nine zoonotic parasites in animal and human populations in the North. Based on a qualitative risk assessment with criteria heavily weighted for human health, these zoonotic parasites are ranked, in the order of decreasing importance, as follows: Echinococcus multilocularis, Toxoplasma gondii, Trichinella and Giardia, Echinococcus granulosus/canadensis and Cryptosporidium, Toxocara, anisakid nematodes, and diphyllobothriid cestodes. Recent and future trends in the importance of these parasites for human health in the North are explored. For example, the incidence of human exposure to endemic helminth zoonoses (e.g. Diphyllobothrium, Trichinella, and Echinococcus) appears to be declining, while water-borne protozoans such as Giardia, Cryptosporidium, and Toxoplasma may be emerging causes of human disease in a warming North. Parasites that undergo temperature-dependent development in the environment (such as Toxoplasma, ascarid and anisakid nematodes, and diphyllobothriid cestodes) will likely undergo accelerated development in endemic areas and temperate-adapted strains/species will move north, resulting in faunal shifts. Food-borne pathogens (e.g. Trichinella, Toxoplasma, anisakid nematodes, and diphyllobothriid cestodes) may be increasingly important as animal products are exported from the North and tourists, workers, and domestic animals enter the North. Finally, key needs are identified to better assess and mitigate risks associated with zoonotic parasites, including enhanced surveillance in animals and people, detection methods, and delivery and evaluation of veterinary and public health services.

Beringia: Intercontinental exchange and diversification of high latitude mammals and their parasites during the Pliocene and Quaternary

ABSTRACT Beringia is the region spanning eastern Asia and northwestern North America that remained ice-free during the full glacial events of the Pleistocene. Numerous questions persist regarding the importance of this region in the evolution of northern faunas. Beringia has been implicated as both a high latitude refugium and as the crossroads (Bering Land Bridge) of the northern continents for boreal mammals. The Beringian Coevolution Project (BCP) is an international collaboration that has provided material to assess the pattern and timing of faunal exchange across the crossroads of the northern continents and the potential impact of past climatic events on differentiation. Mammals and associated parasite specimens have been collected and preserved from more than 200 field sites in eastern Russia, Alaska and northwestern Canada since 1999. Previously, fossils and taxonomic comparisons between Asia and North America mammals have shed light on these events. Molecular phylogenetics based on BCP specimens is now being used to trace the history of faunal exchange and diversification. We have found substantial phylogeographic structure in the Arctic and in Beringia in mustelid carnivores, arvicoline rodents, arctic hares and soricine shrews, including spatially concordant clades and contact zones across taxa that correspond to the edges of Beringia. Among the tapeworms of these mammalian hosts, new perspectives on diversity have also been developed. Arostrilepis horrida (Hymenolepididae) was considered to represent a single widespread and morphologically variable species occurring in a diversity of voles and lemmings in eastern and western Beringia and more broadly across the Holarctic region. The BCP has demonstrated a complex of at least 10 species that are poorly differentiated morphologically. The diversity of Paranoplocephala spp. and Anolocephaloides spp. (Anoplocephalidae) in Beringia included relatively few widespread and morphologically variable species in arvicolines. BCP collections have changed this perspective, allowing the recognition of a series of highly endemic species of Paranoplocephala that demonstrate very narrow host specificity, and additional species complexes among arvicolines. Thus, extensive, previously unrecognized, diversity for tapeworms of 2 major families characterizes the Beringian fauna. By elucidating evolutionary relationships and phylogeographic variation among populations, species and assemblages, refined views of the sequence and timing of biotic expansion, geographic colonization and impact of episodic climate change have been developed for Beringia. Ultimately, Beringia was a determining factor in the structure and biogeography of terrestrial faunas across the Nearctic and Neotropical regions during the Pliocene and Quaternary.

Integrated approaches and empirical models for investigation of parasitic diseases in northern wildlife.

A decade of research has yielded a multidisciplinary approach for detection, prediction, and potential mitigation measures.

Geographic distribution of the muscle-dwelling nematode Parelaphostrongylus odocoilei in North America, using molecular identification of first-stage larvae.

Molecular identification of dorsal-spined larvae (DSL) from fecal samples indicates that the protostrongylid parasite Parelaphostrongylus odocoilei occupies a broader geographic range in western North America than has been previously reported. We analyzed 2,124 fecal samples at 29 locations from thinhorn sheep (Ovis dalli dalli and O. d. stonei), bighorn sheep (Ovis canadensis canadensis and O. c. californiana), mountain goats (Oreamnos americanus), woodland caribou (Rangifer tarandus caribou), mule deer (Odocoileus hemionus hemionus), and black-tailed deer (O. h. columbianus). The DSL were recovered from populations of thinhorn sheep south, but not north, of the Arctic Circle, and they were not recovered from any of the bighorn sheep populations that we examined. In total, DSL were recovered from 20 locations in the United States and Canada (Alaska, Yukon Territory, Northwest Territories, British Columbia, Alberta, and California). The DSL were identified as P. odocoilei by comparing sequences of the second internal transcribed spacer (ITS2) region of ribosomal RNA among 9 protostrongylid species validated by adult comparative morphology. The ITS2 sequences were markedly different between Parelaphostrongylus and other protostrongylid genera. Smaller fixed differences served as diagnostic markers for the 3 species of Parelaphostrongylus. The ITS2 sequences (n = 60) of P. odocoilei were strongly conserved across its broad geographic range from California to Alaska. Polymorphism at 5 nucleotide positions was consistent with multiple copies of the ITS2 within individual specimens of P. odocoilei. This work combines extensive fecal surveys, comparative morphology, and molecular diagnostic techniques to describe comprehensively the host associations and geographic distribution of a parasitic helminth.

The potential impact of climate change on infectious diseases of Arctic fauna.

Abstract Climate change is already affecting Arctic species including infectious disease agents and greater changes are expected. Some infectious diseases are already increasing but future changes are difficult to predict because of the complexity of host-agent-environment relationships. However mechanisms related to climate change that will influence disease patterns are understood. Warmer temperatures will benefit free living bacteria and parasites whose survival and development is limited by temperature. Warmer temperatures could promote survivability, shorter development rates and transmission. Insects such as mosquitoes and ticks that transmit disease agents may also benefit from climate change as well as the diseases they spread. Climate change will have significant impacts on biodiversity. Disease agents of species that benefit from warming will likely become more prevalent. Host species stressed by changing environmental conditions may be more vulnerable to disease agents. Warming could lead to increased agriculture and other economic opportunities in the Arctic bringing people, domestic food animals, pets and invasive species and their disease agents into Northern regions. Climate warming may also favor the release of persistent environmental pollutants some of which can affect the immune system and may favor increased rates of some diseases. (Int J Circumpolar Health 2005; 64(5):468–477)

Protostrongylus stilesi (Nematoda: Protostrongylidae): Ecological Isolation and Putative Host-Switching Between Dall's Sheep and Muskoxen in a Contact Zone

Abstract The occurrence of Protostrongylus stilesi in a population of introduced muskoxen, Ovibos moschatus wardi, on the Arctic Coastal Plain, Yukon Territory (YT) and Northwest Territories (NT), Canada, is consistent with a contemporary colonization event from Dalls sheep, Ovis dalli dalli, which indicates that host specificity may be ecologically based and contextual for this parasite. Colonization of muskoxen by P. stilesi may be a predictable event in zones of sympatry with Dalls sheep; exposure to infection may coincide with occupation of winter ranges of Dalls sheep by muskoxen during the summer season. Disruption of contemporary ecological isolating barriers can result from anthropogenically or climatologically driven habitat perturbation, and result from management practices that influence the distribution of ungulate hosts. Thus, if zones of contact become more extensive or the temporal limits on allopatry are relaxed, we may observe increasing instances of host switching by parasites or pathogens at the interface of newly emerging ecotones. Impacts to northern systems linked to climatologically and anthropogenically driven global change and the effects of management must be tracked within the context of biodiversity survey and inventory and archival collections, as foundations for monitoring ecosystem-level perturbations. A developing interface for muskoxen, wild sheep, and parasites along the Mackenzie River ecotone represents a natural model or field laboratory to examine these processes. Additonally, lungworms, Protostrongylus spp., had not been reported in muskoxen, and a new geographic record for this nematode was established in Dalls sheep from the northern Richardson Mountains, NT.

Emergence of Sylvatic Echinococcus granulosus as a Parasitic Zoonosis of Public Health Concern in an Indigenous Community in Canada

Within a remote Canadian Indigenous community, at least 11* of people had antibodies against Echinococcus granulosus and E. granulosus eggs were detected in 6* of environmentally collected canine fecal samples. Dog ownership, hunting, and trapping were not risk factors for seropositivity, suggesting that people are most likely exposed to E. granulosus through indirect contact with dog feces in the environment. In this situation, human exposure could be most effectively curtailed by preventing consumption of cervid viscera by free-roaming dogs.