Varestrongylus eleguneniensis, Verocai, Kutz, Simard & Hoberg, 2014

Verocai, Guilherme G., Hoberg, Eric P., Simard, Manon, Beckmen, Kimberlee B., Musiani, Marco, Wasser, Sam, Cuyler, Christine, Manseau, Micheline, Chaudhry, Umer N., Kashivakura, Cyntia K., Gilleard, John S. & Kutz, Susan J., 2020, The biogeography of the caribou lungworm, Varestrongylus eleguneniensis (Nematoda: Protostrongylidae) across northern North America, International Journal for Parasitology: Parasites and Wildlife 11, pp. 93-102 : 98

4.2. Absence of Varestrongylus eleguneniensis in caribou herds

Varestrongylus eleguneniensis was not detected in 38 caribou populations. Given the opportunistic nature of our sampling, despite geographically extensive and often relatively site intensive field collections, the true absence of V. eleguneniensis in many of the assessed caribou populations cannot be confirmed. Nevertheless, for some of these herds, various historical and current factors linked to the environment, and the definitive and intermediate host history and ecology, may explain the apparent absence.

Our results provide further evidence for absence of V. eleguneniensis in Greenland caribou, corroborating previous conclusions ( Kutz et al., 2012). In this case, absence may be a result of either parasite loss during or after colonization, or historical absence, i.e. the founder caribou that colonized the region were never infected with the parasite. With respect to parasite loss, this may have been because of host and/or parasite populations being too low to maintain the life-cycle, absence or low numbers of gastropods, or (episodic or constant) unfavorable environmental conditions. A previous study by Steele et al. (2013) hypothesized that the common abomasal nematode of caribou, Ostertagia gruehneri Skrjabin, 1929 , was lost during geographic colonization of the region by caribou approximately 4000–7000 years ago, and subsequently recolonized one of the herds with introduction of infected reindeer to the area. True absence of V. eleguneniensis is also likely for Peary caribou (not sampled in this study) as previously suggested due to climate and probable absence of gastropods on islands of the High Arctic and Greenland ( Kutz et al., 2012). However, the recent emergence of this parasite in muskoxen and caribou on Victoria Island, Nunavut, presumably because of increasingly permissive climatic conditions for parasite development ( Hoberg and Brooks, 2015; Kutz et al., 2013), may facilitate the exposure of Peary caribou to this lungworm in the future ( Kafle et al., 2017a).

Varestrongylus eleguneniensis was not found in Newfoundland caribou; however, these were insufficiently sampled in the present study (n = 11) and need to be more comprehensively assessed. Previous studies on protostrongylid species infecting Newfoundland caribou have relied solely on morphometrics for identification of DSL ( Ball et al., 2001; Lankester and Fong, 1998; Lankester and Northcott, 1979), and also were conducted prior to the discovery and description of V. eleguneniensis ( Kutz et al., 2007; Verocai et al., 2014b). There is considerable overlap in DSL measurement range between V. eleguneniensis [281–400 μm, as per ( Kutz et al., 2007), and 355–394 μm as per ( Kafle et al., 2015)] and P. andersoni [308–382 μm, as per ( Prestwood, 1972)], and to a lesser extent with E. rangiferi [381–490 μm, as per ( Lankester and Northcott, 1979) from caribou with identity of adults confirmed]. Therefore, it is possible that DSL of V. eleguneniensis were misidentified among these of P. andersoni and E. rangiferi , and this minute lungworm may in fact be present in Newfoundland caribou. Conversely, a potential absence of V. eleguneniensis on this island could be due to historical absence within caribou of the North American lineage (NAL) that first colonized the island, or parasite loss after colonization of the island around 12–20 thousand years ago (Ka) ( Yannic et al., 2014).

A recent study suggested that V. eleguneniensis may also be absent from the Atlantic-Gaspésie herd of Quebec ( Turgeon et al., 2018). DSL were found in 9 of 32 sampled caribou and a subsample of these larvae (5 DSL/caribou for 8 animals, 1 DSL for 1 animal) were identified by molecular techniques as P. andersoni . This apparent absence could be explained by either historical absence in founder caribou or loss in modern or recent times. The Gaspésie population, which originates from the NAL caribou lineage, has declined dramatically in modern times and is the only remaining caribou herd south of the Saint Lawrence River ( COSEWIC, 2011; Festa-Bianchet et al., 2011). This loss of connectivity with other caribou populations is a result of extirpation events and habitat fragmentation in the last centuries, and may have impacted the persistence of V. eleguneniensis , if once present. In contrast, P. andersoni seems to have persisted in this herd, which is parapatric with white-tailed deer populations that could have assisted in sustaining this muscle-worm.

Despite a reasonable sample size (n = 122), V. eleguneniensis was not found in any of the five sampled Manitoban herds, including three of the boreal forest ecotype and two of the migratory tundra ecotype. However, the parasite is common in other allopatric and parapatric woodland caribou populations, including populations in the neighboring provinces of Ontario and Saskatchewan ( Festa-Bianchet et al., 2011). One of the Manitoba caribou populations, Norway House, had the highest prevalence of DSL seen among woodland caribou populations (70%), but these all sequenced as P. andersoni . This high DSL prevalence may have masked the presence of V. eleguneniensis in this herd, as we only sequenced larvae (n = 17) from five out of 21 DSLshedding caribou. Regardless of the apparent absence of V. eleguneniensis in the sampled woodland caribou populations in Manitoba, the parasite is present in northern areas of that province, as it occurs in both the Beverly and Qamanirjuaq barren-ground herds ( Kutz et al., 2007, present study). The winter range of the Qamanirjuaq herd partially overlaps with the Cape Churchill woodland caribou, whose range partially overlaps with the Pen Island herd. Therefore, there is potential for the presence of V. eleguneniensis in these herds, despite it not being detected in the current study.