Perspective Chapter: The Potential Role of Nematode Parasites in Wildlife Decline – Evidence from Allegheny Woodrats (Neotoma magister), Northern Flying Squirrels (Glaucomys sabrinus) and Now the Eurasian Red Squirrel (Sciurus vulgaris)

Abstract

Climate change and habitat loss alter the landscape for wildlife, resulting in shifts in geographic ranges, occupation of smaller, remnant habitat patches, or use of novel environments. These processes often lead to sympatry between species that historically were non-sympatric. Such interactions increase competition for resources and expose species to novel parasites that reduce a species’ fitness leading to wildlife declines. We explore these interactions in species of endangered North American rodents—Northern flying squirrels (Glaucomys sabrinus) and Allegheny woodrats (Neotoma magister). Northern flying squirrels are declining in the United States due to competition with its congener, southern flying squirrels (Glaucomys volans). Evidence indicates that competition is mediated by a shared nematode, Strongyloides robustus. Transmission of this nematode to northern flying squirrels is increasing due to forest fragmentation and climate change. We also note the recent discovery of S. robustus as a novel parasite and a factor in the decline of the European red squirrel (Sciurus vulgaris). Likewise, in Allegheny woodrats, shrinking landscape changes have resulted in increased range overlap with raccoons (Procyon lotor) that harbor a nematode fatal to woodrats. The subsequent transmission of this nematode, Baylisascaris procyonis, to woodrats is a contributing factor to woodrat decline throughout the Appalachians.

1. Introduction

Global climate change and human-induced habitat loss alter the landscape for native wildlife, resulting in shifts in geographic ranges, occupation of smaller, remnant habitat patches, or use of novel or new environments. These processes often lead to sympatry between species that historically occupied non-overlapping ranges and habitats. Such interactions may result in increased competition for resources and expose species to novel parasites that adversely affect a species’ fitness leading to wildlife declines. For example, if the distribution of a host species shifts, so too will the distribution of its parasites. Therefore, in some ecosystems, invasive and endemic hosts may experience new parasites which may be pathogenic to naïve hosts [1, 2].

Species may shift their distribution as a response to changing climate but some species also may be introduced incidentally or purposefully by human activities –resulting in similar novel host-parasite interactions [3]. For instance, global trade, transport, and the introduction of exotic species likely facilitates parasite-mediated competition between species. These trends may worsen under climate change because new species assemblages may occur, thus creating opportunities for parasite exchange. When previously allopatric host species come into sympatry, novel host–parasite interactions may emerge if parasites are able to successfully infect newly exposed hosts [4]. These parasitic ‘co-invaders’ may mediate the impacts of biological introductions by potentially amplifying transmission to native species [3]. However, evaluating threats from introduced parasites to native wildlife is difficult due to limited information associated with distribution shifts or introductions [5]. Complicating these interactions, climate change may alter parasite survival, development rates, and periods of transmission between intermediary hosts [2]. We explore these interactions and concurrent species declines in several species of wild rodents demonstrating conservation challenges in a globalizing planet experiencing climate change.

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, 7, 8, 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 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].

Figure 1.

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

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 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.

3. Baylisascaris procyonis in raccoons and Allegheny woodrats: nematode-acerbated mammal decline

Ascarids are host-specific nematodes (order Ascaridida, class Secernentea) that are parasitic in the intestines of various terrestrial vertebrates. Adult ascarids live in the small intestine of their definitive host and produce eggs which are shed in the feces. Eggs are very resistant to environmental extremes and can remain infective in the environment for many years [19, 20]. Like other ascarids, B. procyonis has a direct and indirect life cycle and can cause zoonotic infection in a variety of paratenic hosts [20]. Although raccoon (Procyon lotor) is the specific host for the adult worm, there is no obligatory intermediate host. Adult female worms in the small intestines of raccoons collectively shed millions of eggs per day which are passed in the hosts’ feces. After being passed, Baylisascaris eggs continue to develop and an infectious larva develops in 2–4 weeks. Raccoons become infected by ingesting B. procyonis eggs or larva during social feeding or grooming activities. In addition, raccoons may become infected by consuming flesh or droppings of other vertebrates (specifically mammals or birds) that have become infected by this roundworm. B. procyonis is common (prevalence rates ~65%) throughout North American wherever raccoons are found. Except for heavy infections, B. procyonis causes no disease in their primary host [20].

Although raccoons are the natural host for B. procyonis, other mammals and birds can become aberrant intermediate hosts after inadvertently ingesting eggs containing infectious larva. In these aberrant hosts, B. procyonis causes severe central nervous system disease that is often fatal. The life history of raccoons may contribute to the inadvertent transmission of Baylisascaris to non-raccoon species. Raccoon defecate in common latrines resulting in a high abundance and concentration of B. procyonis eggs that remain infectious for months due to their resistance to environmental extremes [19, 20].

Allegheny woodrat is a species of new world rodent that is endemic to the Appalachian mountains of eastern North America [21, 22, 23]. A decline in the numbers and range of the Allegheny woodrat was first noticed in the 1960s and the decline was considered severe by the mid-1970s. The species has since been extirpated from New York and Connecticut. Extensive surveys in Pennsylvania have revealed that woodrats have disappeared from approximately one third of their former range there [21]. Similar declines have been noted in Maryland and Ohio. Allegheny woodrat populations remained stable in West Virginia but recent data indicates that populations are declining in that state as well. This rapid decline has led to the species being listed as endangered and/or threatened by states throughout its range and is currently considered a species of conservation interest and protection by the U.S. Forest Service – although it is not listed under the Endangered Species Act [24].

Allegheny woodrats typically occur in rocky areas associated with forested mountain ridges such as cliffs, caves, talus slopes and rocky fissures. The rocky barrens where they den are generally devoid of vegetation with the exception of the occasional tree that manages to survive among the rocks. Active primarily at night, woodrats leave the security of their rocky dens to visit adjacent areas to feed on the available vegetation. They are typically found in talus fields having large sized boulders (greater than 1.2 m in diameter). Vegetative associations include birch (Betula spp.)/chestnut oak (Quercus prinus) forests, scattered birch, oaks and shrubs with herbaceous plants at the base of slopes.

Allegheny woodrats exhibit behaviors that are typical of a ‘pack rat’ and, besides food items, woodrats also collect and store various non-food items (e.g., feathers, snail shell, dried leaves, human items) in their rocky dens. The foraging behavior of Allegheny woodrats may increase their susceptibility to encountering Baylisascaris in the feces of raccoons. For example, woodrats may forage for and collect seeds present in the dried feces found in raccoon latrines. Woodrats may make repeated visits to these latrine sites, collect seeds, and subsequently store them in their food caches—resulting in repeated exposure to the parasite [21, 23].

Exposure to raccoon roundworm is considered one of many factors that act synergistically to cause the decline of this native rodent [23]. At raccoon latrine sites associated with woodrats, published prevalence rates of B. procyonis vary from 11% (Indiana), 22% (Maryland), and 33% (Pennsylvania) [22, 25, 26]. Accordingly, at sites where woodrats persist, raccoon roundworm was absent [22]. Furthermore, forest fragmentation and raccoon densities are also lower than at sites where woodrats have been extirpated [26, 27, 28]. In New York state, an unsuccessful woodrat reintroduction effort in 1990 was attributed to high prevalence of raccoons and Baylisascaris at the reintroduction site [29]. Additionally, in Indiana woodrat translocations failed at one site where the presence of raccoons and Baylisascaris was high [27]. However, the distribution of anhelminitic baits reduced levels of roundworm contamination permitting persistence of woodrats at additional translocation sites in Indiana [27].

Woodrat translocations should be considered at formerly-occupied sites if raccoon latrines and B. procyonis are removed. Anhelminitic baits can be used to reduce roundworm prevalence rates at these sites and the maintenance of continuous, mature deciduous forested habitat will reduce raccoon densities. Furthermore, protecting sites where woodrats persist from habitat alterations that will attract raccoons is important. A comprehensive regional approach to assessing the prevalence of B. procyonis in raccoons and the exposure level to infection in woodrat habitat is necessary. Once prevalence rates are more widely-understood, the feasibility of using anhelminitic approaches in core woodrat areas can be considered. Finally, the effects of human encroachment (highways, urban areas, agriculture) forest fragmentation on raccoon densities and woodrat habitat needs to be better understood [21]. A compilation of resources related to Allegheny woodrats, including the effects of B. procyonis, is available at: https://library.delval.edu/allegheny-woodrats/conservation.

4. Conclusions

Here we described two nematode parasites, Strongyloides robustus and B. procyonis, relatively common in one mammalian host that contribute to decline in another neighboring mammal species of special conservation concern. Where southern and northern flying squirrels are sympatric, S. robustus (commonly found in southern species) appears to contribute to poor health in threatened/endangered northern flying squirrels. Recently, S. robustus, also found in the invasive Eastern gray squirrel in Europe, appears to be transmitted to the now threatened Eurasian red squirrel and may contribute to its decline by modifying its behavior and limiting its ability to compete with its congener. Similarly, B. procyonis a common roundworm of the raccoon is often contracted by the Allegheny woodrat an inhabitant of rocky habitats on forested mountain ridges of the eastern and central U.S.A. where it feeds on and stores seeds deposited in the feces of raccoons deposited in latrines often associated with woodrat habitat. Now lost from more than a third of their original range, decline of the Allegheny woodrat is attributed largely to the presence of raccoons and this roundworm parasite.

Species distribution changes and range shifts due to climate change and/or human activity will result in the emergence of new species assemblages. Within these new assemblages, species may affect each other directly through predation or competition, or indirectly by habitat alteration or restructuring host-parasite interactions [3]. The role of climate change in restructuring host–parasite interactions through shifts in host ranges is poorly understood [4] but case studies in rodents presented here provide some predictions about the potential conservation challenges that may emerge.

Acknowledgments

We thank the Pennsylvania Game Commission, Pennsylvania Department of Conservation and Natural Resources, Wild Resources Conservation Program, State Wildlife Grants Program, Northeast Association of Fish and Wildlife Agencies, Penn State Altoona, and Wilkes University for financial support of our research. We thank John Young, U.S. Geological Survey, for creating Figure 1. In addition, we thank Gregory Turner, Pennsylvania Game Commission, and Dr. Peter Hudson, Huck Institutes, Penn State University, for creative leadership and insight into the interactions of wildlife and parasites.

Conflict of interest

The authors declare no conflict of interest.