**2.** *Strongyloides robustus* **parasite-mediated competition in squirrels in North American and Europe**

*Strongyloides robustus* is an intestinal nematode reported to occur in several squirrel species (Sciuridae) across at least two continents. Documented hosts include the Eastern gray squirrel (*Sciurus carolinensis*), southern flying squirrels (*Glaucomys volans*), northern flying squirrel (*Glaucomys sabrinus*), and the North American red squirrel (*Tamiasciurus hudsonicus*) in North America as well as the invasive Eastern gray squirrels in Europe and now as a spill-over parasite in Europe's native red squirrel (*Sciurus vulgaris*) [6–9].

*Strongyloides robustus* exhibits a direct life cycle whereby eggs are shed and hatch, usually within a few days depending on ambient temperature, developing first as a larval (L1) stage, a second, L2 stage (a rhabdidiform larvae) and finally an infective, L3 stage (filariform larvae) [8]. Infection, which results from direct consumption of the L3 larvae, is assumed to occur most often in the nest and may be transmitted from one species to another when nest use overlaps over a relatively short time period [8, 9].

Across North America the two flying squirrel species, in which this nematode occurs, are largely allopatric with *G. sabrinus* occupying mostly coniferous forests (spruce [*Picea* sp.] and fir [*Abies* sp.]) of boreal regions of the United States of America (U.S.A.) and Canada and *G. volans* occurring in hardwood forests of the

#### *Perspective Chapter: The Potential Role of Nematode Parasites in Wildlife Decline – Evidence... DOI: http://dx.doi.org/10.5772/intechopen.103119*

midwest, east and southeastern U.S.A. However, there are regions in the Appalachian Mountains and areas northward of the eastern U.S.A. where the ranges of the two species exhibit limited sympatry and may compete for nest sites (**Figure 1**). Although both species consume seeds and nuts [7], *G. sabrinus* relies on a steady diet of fungi and lichens throughout most of its range, whereas *G. volans* is generally limited to hardwood stands where it feeds on the nuts of hardwood species. Although these habitat differences and dietary limitations maintain allopatry across much of their range, mixed stands, especially in the east and northeast, often bring the two species together where the edges of each species' range meet. In addition, forest fragmentation due to human-mediated landscape changes has reduced coniferous patches in these regions, permitting *G. volans'* and *G. sabrinus'* ranges to overlap [10]. Furthermore, global climate change has expanded *G. volans'* range northward and increased interactions between these two species [11].

For several decades now, there has been growing circumstantial evidence that *S. robustus* may mediate competitive interactions between the two species of flying squirrels in North America [6, 12]. *G. volans* a common host for *S. robustus* shows no evidence of pathology when infected with this nematode, whereas *G. sabrinus* may be quite negatively affected and even killed by the parasite [6, 13, 14].

Based on these early circumstantial but compelling studies [6, 7], Price et al. [12] included these studies on flying squirrels in their comprehensive examination of parasite-mediated competition between similar pairs of species. They proposed two hypotheses to potentially explain how parasites of one host are likely to negatively impact a

#### **Figure 1.**

*Distribution of Northern flying squirrel (*Glaucomys sabrinus*) and Southern flying squirrel (*Glaucomys volans*) in the United States, 2021.*

closely related host. In the first, the geographic range hypothesis, they predicted that species of larger geographic ranges carry more parasites and are therefore more likely to displace a similar species with a smaller range. In the second, the body-size hypothesis, Price et al. [12] hypothesize that smaller species with higher densities and higher rates of population growth are likely to displace the larger bodied species. The second hypothesis was supported in 12 of 15 cases, one of which included *G. volans* and *G. sabrinus.*

Krichbaum et al. [15] conducted a survey of gut parasite communities in sympatric populations of the two species of flying squirrel in Pennsylvania and populations of *G. sabrinus* in New York where *G. volans* is not found. Where sympatric, both flying squirrel species hosted *S. robustus* with the southern flying squirrels showing substantial numbers of the parasite and exhibiting an overdispersed distribution in the host (*G. volans*). Populations of northern flying squirrels in northern New York were not infected with *S. robustus*.

In tests of the immuno-competence hypothesis that higher levels of testosterone increase susceptibility to parasites, Waksmonski et al. [16] used high performance liquid-chromatography-ultra-violet spectroscopy (HPLC-UV) to compare testosterone levels in both species of flying squirrels infected with *S. robustus*. They observed strong qualitative evidence that testosterone levels were substantially higher in northern flying squirrels hosting *S. robustus* compared with southern flying squirrels hosting the parasite.

Even stronger evidence for repeated contact between these two species in Pennsylvania and Ontario is reported by Garroway et al. [11]. In Pennsylvania, for example, both species of Glaucomys were first captured in the same nest [14]. Soon thereafter, following an unseasonably warm period, *G. volans* was observed to move northward in Ontario and Pennsylvania, mate and produce hybrid offspring [11]. This evidence of hybridization clearly documents significant contact between the two species in the same nests where exchange of S*. robustus* is likely to occur.

Recent studies in a similar system suggest that the invasive Eastern gray squirrel in Europe [17], which is a common host for *S. robustus* may share this parasite with the endangered Eurasian red squirrel (*S. vulgaris*), potentially causing negative health effects [18]. In fact, this study represents the first experimental investigation documenting the negative effects of *S. robustus* on a potentially vulnerable host. Romeo et al. [18] conducted boldness/activity tests of individual Eurasian red squirrels infected with S*. robustus*, captured at sites where the invasive gray squirrel was found and at control sites where *S. vulgaris* was the only squirrel present. Based on these studies observers documented a negative association between the red squirrels' activity level (boldness) and infection with the invasive parasite at sites of sympatry.

Collectively the above studies provide strong evidence that *S. robustus* may mediate competition between *G. volans* and *G*. *sabrinus* in parts of North America and between populations of the invasive *S. carolinensis* and the native *S. vulgaris* in Europe. In both systems the affected species are considered species of conservation concern and listed as endangered in those parts of their range where *S. robustus* is potentially exerting its greatest effect.
