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.
- Allegheny woodrat
- flying squirrels
- Eastern gray squirrels
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 . 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 . These parasitic ‘co-invaders’ may mediate the impacts of biological introductions by potentially amplifying transmission to native species . However, evaluating threats from introduced parasites to native wildlife is difficult due to limited information associated with distribution shifts or introductions . Complicating these interactions, climate change may alter parasite survival, development rates, and periods of transmission between intermediary hosts . We explore these interactions and concurrent species declines in several species of wild rodents demonstrating conservation challenges in a globalizing planet experiencing climate change.
Strongyloides robustusparasite-mediated competition in squirrels in North American and Europe
Across North America the two flying squirrel species, in which this nematode occurs, are largely allopatric with
For several decades now, there has been growing circumstantial evidence that
Based on these early circumstantial but compelling studies [6, 7], Price et al.  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.  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
Krichbaum et al.  conducted a survey of gut parasite communities in sympatric populations of the two species of flying squirrel in Pennsylvania and populations of
In tests of the immuno-competence hypothesis that higher levels of testosterone increase susceptibility to parasites, Waksmonski et al.  used high performance liquid-chromatography-ultra-violet spectroscopy (HPLC-UV) to compare testosterone levels in both species of flying squirrels infected with
Even stronger evidence for repeated contact between these two species in Pennsylvania and Ontario is reported by Garroway et al. . In Pennsylvania, for example, both species of Glaucomys were first captured in the same nest . Soon thereafter, following an unseasonably warm period,
Recent studies in a similar system suggest that the invasive Eastern gray squirrel in Europe , which is a common host for
Collectively the above studies provide strong evidence that
Baylisascaris procyonisin raccoons and Allegheny woodrats: nematode-acerbated mammal decline
Although raccoons are the natural host for
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 . 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 .
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 (
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
Exposure to raccoon roundworm is considered one of many factors that act synergistically to cause the decline of this native rodent . At raccoon latrine sites associated with woodrats, published prevalence rates of
Woodrat translocations should be considered at formerly-occupied sites if raccoon latrines and
Here we described two nematode parasites,
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 . The role of climate change in restructuring host–parasite interactions through shifts in host ranges is poorly understood  but case studies in rodents presented here provide some predictions about the potential conservation challenges that may emerge.
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.
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