Range expansion of muskox lungworms track rapid arctic warming: implications for geographic colonization under climate forcing

Rapid climate warming in the Arctic results in multifaceted disruption of biodiversity, faunal structure, and ecosystem health. Hypotheses have linked range expansion and emergence of parasites and diseases to accelerating warming globally but empirical studies demonstrating causality are rare. Using historical data and recent surveys as baselines, we explored climatological drivers for Arctic warming as determinants of range expansion for two temperature-dependent lungworms, Umingmakstrongylus pallikuukensis and Varestrongylus eleguneniensis, of muskoxen (Ovibos moschatus) and caribou (Rangifer tarandus), in the Canadian Arctic Archipelago from 1980 through 2017. Our field data shows a substantial northward shift of the northern edge of the range for both parasites and increased abundance across the expanded ranges during the last decade. Mechanistic models parameterized with parasites’ thermal requirements demonstrated that geographical colonization tracked spatial expansion of permissive environments, with a temporal lag. Subtle differences in life histories, thermal requirements of closely related parasites, climate oscillations and shifting thermal balances across environments influence faunal assembly and biodiversity. Our findings support that persistence of host-parasite assemblages reflects capacities of parasites to utilize host and environmental resources in an ecological arena of fluctuating opportunity (alternating trends in exploration and exploitation) driving shifting boundaries for distribution across spatial and temporal scales

Parasites of an Arctic scavenger; the wolverine (Gulo gulo)

Parasites are fundamental components within all ecosystems, shaping interaction webs, host population dynamics and behaviour. Despite this, baseline data is lacking to understand the parasite ecology of many Arctic species, including the wolverine (Gulo gulo), a top Arctic predator and scavenger. Here, we combined traditional count methods (i.e. adult helminth recovery, where taxonomy was confirmed by molecular identification) with 18S rRNA high-throughput sequencing to document the wolverine parasite community. Further, we investigated whether the abundance of parasites detected using traditional methods were associated with host metadata, latitude, and longitude (ranging from the northern limit of the boreal forest to the low Arctic and Arctic tundra in Nunavut, Canada). Adult parasites in intestinal contents were identified as Baylisascaris devosi in 72% (n = 39) of wolverines and Taenia spp. in 22% (n = 12), of which specimens from 2 wolverines were identified as T. twitchelli based on COX1 sequence. 18S rRNA high-throughput sequencing on DNA extracted from faeces detected additional parasites, including a pseudophyllid cestode (Diplogonoporus spp. or Diphyllobothrium spp.), two metastrongyloid lungworms (Angiostrongylus spp. or Aelurostrongylus spp., and Crenosoma spp.), an ascarid nematode (Ascaris spp. or Toxocara spp.), a Trichinella spp. nematode, and the protozoan Sarcocystis spp., though each at a prevalence less than 13% (n = 7). The abundance of B. devosi significantly decreased with latitude (slope = -0.68; R2 = 0.17; P = 0.004), suggesting a northerly limit in distribution. We describe B. devosi and T. twitchelli in Canadian wolverines for the first time since 1978, and extend the recorded geographic distribution of these parasites ca 2000 km to the East and into the tundra ecosystem. Our findings illustrate the value of molecular methods in support of traditional methods, encouraging additional work to improve the advancement of molecular screening for parasites

Hiding in plain sight: discovery and phylogeography of a cryptic species of Trichinella (Nematoda: Trichinellidae) in wolverine (Gulo gulo)

Understanding parasite diversity and distribution is essential in managing the potential impact of para- sitic diseases in animals and people. Imperfect diagnostic methods, however, may conceal cryptic species. Here, we report the discovery and phylogeography of a previously unrecognized species of Trichinella in wolverine (Gulo gulo) from northwestern Canada that was indistinguishable from T. nativa using the stan- dard multiplex PCR assay based on the expansion segment 5 (ESV) of ribosomal DNA. The novel genotype, designated as T13, was discovered when sequencing the mitochondrial genome. Phylogenetic analyses of the mitochondrial genome and of 15 concatenated single-copy orthologs of nuclear DNA indicated a com- mon ancestor for the encapsulated clade is shared by a subclade containing Trichinella spiralis and Trichinella nelsoni, and a subclade containing T13 and remaining taxa: T12 + (T2 + T6) + [(T5 + T9) + (T 3 + T8)]. Of 95 individual hosts from 12 species of mammalian carnivores from northwestern Canada from which larvae were identified as T. nativa on multiplex PCR, only wolverines were infected with T13 (14 of 42 individuals). These infections were single or mixed with T. nativa and/or T6. Visual examination and motility testing confirmed that T13 is encapsulated and likely freeze-tolerant. We developed a new Polymerase Chain Reaction-Restriction Fragment Length Polymorphism which unequivocally distinguishes between T13 and T. nativa. We propose Trichinella chanchalensis n. sp. for T13, based on significant genetic divergence from other species of Trichinella and broad-based sampling of the Trichinella genome. Exploration of Alaskan and Siberian isolates may contribute to further resolution of a phylogeo- graphically complex history for species of Trichinella across Beringia, including Trichinella chanchalensis n. sp. (T13

Muskox Health Ecology Symposium 2016: Gathering to Share Knowledge on Umingmak in a Time of Rapid Change

The Muskox, Ovibos moschatus, also known as Umingmak ‘the Bearded One,’ is a taxonomically unique, cold-adapted, ice-age survivor. Originally native to Canada and Greenland, it has established a circum-Arctic distribution via introduced populations. As a key resident herbivore in northern ecosystems, the muskox has importance that should not be underestimated. Muskoxen play an important role in the cultural identity of Arctic Indigenous peoples and provide a healthy source of country food. More recently, recognition of the economic potential of the species through tourism, sport hunting, and the traditional sale of handicrafts has generated renewed interest in muskoxen and their ecology. Recent documentation of diseases, including several zoonoses, regional mortality events, and population declines have highlighted knowledge gaps in both our understanding of the drivers of muskox population fluctuations and the potential sensitivity of this species to a rapidly changing climate (Kutz et al., 2013, 2015; Handeland et al., 2014; Ytrehus et al., 2015; Tomaselli et al., 2016c; Afema et al., 2017)

Climate Change and Range Expansion of Protostrongylid Nematodes in the Canadian Arctic

Through this doctoral research, I aimed to determine the diversity, distribution and abundances of protostrongylids in muskoxen and caribou from several sites in Subarctic and Arctic Canada and investigate the northward range expansion of Umingmakstrongylus pallikuukensis and Varestrongylus eleguneniensis in relation to Arctic warming. I first developed morphological keys to differentiate the first stage larvae (L1) of U. pallikuukensis, V. eleguneniensis and Parelaphostrongylus andersoni. This enabled me to identify L1 to the species level and determine the intensity of infections. Secondly, I analyzed over 1600 muskox and caribou fecal samples, and 40 muskox lung samples to determine the diversity, distribution and abundance patterns of protostrongylids. I found that the diversity and abundance of protostrongylids varied geographically. Both U. pallikuukensis and V. eleguneniensis had expanded their ranges and increased in abundance on Victoria Island between 2013 and 2017, with U. pallikuukensis expanding its range faster than V. eleguneniensis. I also detected P. andersoni in the Dolphin and Union caribou herd. In the third part of the study, I determined the important life cycle parameters for U. pallikuukensis and V. eleguneniensis through lab experiments. I demonstrated that V. eleguneniensis has higher thermal requirements for larval development inside the intermediate host, a shorter prepatent and patent period, and lower fecundity than U. pallikuukensis. Based on these findings I hypothesized that higher thermal requirements and lower fecundity might be limiting the rate and extent of range expansion for V. eleguneniensis. Finally, to map the thermal niches of U. pallikuukensis and V. eleguneniensis from 1980 through to 2017, I parametrized a process-based mechanistic model (Degree-day model) using data derived from the lab experiments, the literature, and high-resolution temperature data from a regional climate model. Models indicated a substantial expansion in the zones of climatic suitability for both parasites during the study period with the realized niches of both parasites lagging behind the expansion of their thermal niches. This work contributes to the field of Arctic parasitology by providing simple and effective diagnostic tools for protostrongylids, and adding to the present knowledge on diversity, distribution, abundance as well as ecology of protostrongylid nematodes. Finally, by using a multifaceted approach to investigate the patterns of parasite emergence in the Arctic, this study contributes to the overall understanding of disease emergence in a rapidly changing ecosystem

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

Abstract 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

Morphological and morphometric differentiation of dorsal-spined first stage larvae of lungworms (Nematoda: Protostrongylidae) infecting muskoxen (Ovibos moschatus) in the central Canadian Arctic

Umingmakstrongylus pallikuukensis and Varestrongylus eleguneniensis are the two most common protostrongylid nematodes infecting muskoxen in the North American Arctic and Subarctic. First stage larvae (L1) of these lungworms have considerable morphological similarity that makes their differential diagnosis very difficult. Using light microscopy, we studied in detail the L1 of these two species and identified the key differences in morphological and morphometric attributes. Thirty L1 of each species from naturally infected muskox were heat-killed and then assessed for morphological and morphometric features that could be used for species-level differentiation. Key differentiating features include: length and morphology of the tail extension, curvature of the body, ventral post-anal transverse cuticular striations, and total body length. A laboratory guide for differentiation of L1 based on these species-specific characters was prepared and used by an experienced observer to identify an additional 35 L1 extracted from a different set of fecal samples from free-ranging muskoxen with mixed infections. The identities of these L1 were confirmed by sequence analysis of the ITS-2 region of the nuclear ribosomal DNA. Accuracy of morphological identification was 100 percent, reflecting the reliability of the proposed guide for differentiation. Using the guide, three minimally trained lab assistants each fixed and accurately identified 10 of 10 randomly selected L1. Ability to morphologically differentiate these facilitates the monitoring of overlapping range expansion of both parasites in the Canadian Arctic. Studies enabling species-level parasite identification are also critical for defining biodiversity, detecting mixed infections, and understanding host–parasite interactions. Morphological identification is a simple, reliable and cost-effective alternative to labor and equipment intensive molecular methods and can easily be performed in low resource settings

Morphological keys to advance the understanding of protostrongylid biodiversity in caribou (Rangifer spp.) at high latitudes

The Protostrongylidae is a diverse family of nematodes capable of causing significant respiratory and neuromuscular disease in their ungulate and lagomorph hosts. Establishing the species diversity and abundance of the protostrongylid fauna has been hindered because the first stage larvae, commonly referred as dorsal spined larvae (DSL), that are shed in the feces are morphologically very similar among several genera. We aimed to determine the protostrongylid diversity and distribution in caribou (Rangifer tarandus groenlandicus and R. t. pearyi) in the central and high Canadian Arctic. We first developed, tested and validated a morphological diagnostic guide for the DSL of two important protostrongylids, Parelaphostrongylus andersoni and Varestrongylus eleguneniensis, and then applied this guide to determine the prevalence and intensity of infection of these parasites in fecal samples from 242 caribou. We found that DSL of V. eleguneniensis and P. andersoni can be differentiated morphologically based on the structural differences at the caudal extremity. The presentation and morphology of the dorsal spine, and caudoventral bulging at the start of the tail extension were identified as the key identifying features. The two species were found in caribou on the arctic mainland and southern Victoria Island in single and co-infections, but the prevalence and intensity of infection was low. No protostrongylids were detected in caribou from the high arctic islands. Through this study, we provide a simple, efficient, and robust method to distinguish the DSL of the two protostrongylids, and present the current status of infection in different herds of caribou of the central Canadian Arctic. We report new geographic and host records for P. andersoni infection in Dolphin and Union caribou herd. Keywords: Parelaphostrongylus andersoni, Varestrongylus eleguneniensis, Diagnostic parasitology, Morphological diagnosis, Dorsal spined larvae, Canadian Arctic, Dolphin and Union caribo