Susan J. Kutz

Climate Change and Infectious Diseases: From Evidence to a Predictive Framework

Scientists have long predicted large-scale responses of infectious diseases to climate change, giving rise to a polarizing debate, especially concerning human pathogens for which socioeconomic drivers and control measures can limit the detection of climate-mediated changes. Climate change has already increased the occurrence of diseases in some natural and agricultural systems, but in many cases, outcomes depend on the form of climate change and details of the host-pathogen system. In this review, we highlight research progress and gaps that have emerged during the past decade and develop a predictive framework that integrates knowledge from ecophysiology and community ecology with modeling approaches. Future work must continue to anticipate and monitor pathogen biodiversity and disease trends in natural ecosystems and identify opportunities to mitigate the impacts of climate-driven disease emergence.

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.

Ecological Consequences of Sea-Ice Decline

After a decade with nine of the lowest arctic sea-ice minima on record, including the historically low minimum in 2012, we synthesize recent developments in the study of ecological responses to sea-ice decline. Sea-ice loss emerges as an important driver of marine and terrestrial ecological dynamics, influencing productivity, species interactions, population mixing, gene flow, and pathogen and disease transmission. Major challenges in the near future include assigning clearer attribution to sea ice as a primary driver of such dynamics, especially in terrestrial systems, and addressing pressures arising from human use of arctic coastal and near-shore areas as sea ice diminishes.

Structure, biodiversity, and historical biogeography of nematode faunas in holarctic ruminants: morphological and molecular diagnoses for Teladorsagia boreoarcticus n. sp. (Nematoda: Ostertagiinae), a dimorphic cryptic species in muskoxen (Ovibos moschatus).

Discovery of the ostertagiine nematode Teladorsagia boreoarcticus n. sp. in muskoxen, Ovibos moschatus, from the central Canadian Arctic highlights the paucity of knowledge about the genealogical and numerical diversity of nematode faunas characteristic of artiodactyls at high latitudes across the Holarctic. Teladorsagia boreoarcticus is a dimorphic cryptic species distinguished from Teladorsagia circumcincta/Teladorsagia trifurcata in domestic sheep by a 13% divergence in the ND4 region of mitochondrial DNA, constant differences in the synlophe, and significantly longer esophageal valve, spicules, gubernaculum, and bursa. Teladorsagia boreoarcticus represents an archaic component of the North American fauna and may have a Holarctic distribution in muskoxen and caribou. Recognition of T. boreoarcticus in muskoxen, in part, corroborates hypotheses for the existence of a cryptic species complex of Teladorsagia spp. among Caprinae and Cervidae at high latitudes and indicates the importance of climatological determinants during the late Tertiary and Pleistocene on diversification of the fauna. Also reinforced is the concept of the North American fauna as a mosaic of endemic and introduced species. Discovery of a previously unrecognized species of Teladorsagia has additional implications and clearly indicates that (1) our knowledge is incomplete relative to potentially pathogenic nematodes that could be exchanged among domestic and wild caprines; (2) we do not have sufficient knowledge of the fauna to understand the ecological control mechanisms (limitations) on dissemination and host range; and (3) an understanding of historical and geographical influences on the genealogical diversity and distribution of nematode faunas in domestic and wild ruminants is requisite to define the interface between agricultural and natural ecosystems across the Holarctic.

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.

“Emerging” Parasitic Infections in Arctic Ungulates

Abstract Important drivers for emergence of infectious disease in wildlife include changes in the environment, shrinking habitats or concentration of wildlife, and movement of people, animals, pathogens, or vectors. In this paper we present three case-studies of emerging parasitic infections and diseases in ungulates in the Canadian north. First we discuss climate warming as an important driver for the emergence of disease associated with Umingmakstrongylus pallikuukensis, a nematode lungworm of muskoxen. Then we examine how Protostrongylus stilesi, the sheep lungworm, emerged (or re-emerged) in muskoxen after re-introduction of this host into its historical range made it sympatric with Dalls sheep. Finally, we consider Teladorsagia boreoarcticus, a newly described and common abomasal nematode of muskoxen that is emerging as a disease-causing parasite and may be an important regulator for muskox populations on Banks Island, Northwest Territories. These and other arctic host-parasite systems are exquisitely tuned and constrained by a harsh and highly seasonal environment. The dynamics of these systems will be impacted by climate change and other ecological disruptions. Baseline knowledge of parasite biodiversity and parasite and host ecology, together with predictive models and long-term monitoring programs, are essential for anticipating and detecting altered patterns of host range, geographic distribution, and the emergence of parasitic infections and diseases.

Dogs as Sources and Sentinels of Parasites in Humans and Wildlife, Northern Canada

A minimum of 11 genera of parasites, including 7 known or suspected to cause zoonoses, were detected in dogs in 2 northern Canadian communities. Dogs in remote settlements receive minimal veterinary care and may serve as sources and sentinels for parasites in persons and wildlife, and as parasite bridges between wildlife and humans.

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.

Crossing the Interspecies Barrier: Opening the Door to Zoonotic Pathogens

This research was funded by EU FP7 grant ANTIGONE (#278976). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.