The Invasive Bank Vole (Myodes glareolus): A Model System for Studying Parasites and Ecoimmunology during a Biological Invasion, McManus et al. Animals 2021. Read it here.
Emerging infectious diseases, biological invasions & rodents
Over the past century, there has been an increase in Emerging Infectious Diseases (EIDs), leading to outbreaks in diseases of zoonotic origin, such as SARS-CoV, MERS-CoV, Lassa, Zika, Ebola, HIV, and not to forget the ongoing Covid-19 pandemic. The increase in these EID events have been linked to the increasing rate of environmental change, including habitat destruction and biological invasions.
While EIDs are considered a major risk to human populations, they can also be detrimental to indigenous wildlife. For example, it has been suggested that the introduced grey squirrel (Sciurus carolinensis), has resulted in the transfer of squirrelpox (Parapoxvirus) to the indigenous red squirrel (Sciurus vulgaris). Consequently, the introduction of non-native invaders can affect native species through more cryptic means than direct competition, by altering the pathogen communities present in the native species. This can manifest through a number of mechanisms, the most obvious of which is spillover. Spillover occurs when a non-native parasite co-invades with the non-native host species, spreading to the immunologically naïve native (as in the case of the red and grey squirrels). Conversely, a less obvious mechanism by which introduced species affect pathogen communities is spillback. Spillback occurs when the non-native host has an increased competency for a native parasite resulting in an amplification effect: the native parasite multiplies in the introduced species, but the native host suffers more from the increased number of parasites in its environment. Of course, benign impacts on native species’ relationships with pathogens are also possible. The non-native host can also have a lower competency for a native parasite, thus diluting the parasite burden of the native species. (Dunn and Hatcher explain these mechanisms in much more detail here, if you are curious to know more.)
Wild rodents have offered key insights into disease ecology. For example, Laakkonen et al. demonstrated that Eimeria infections in vole populations show seasonal cycles peaking in autumn, while similar studies on Puumala orthohantavirus have shown the virus to cycle in bank vole populations with peak infection occurring in spring. Their worldwide distribution and ability to spread with human activity make rodents excellent models for understanding disease ecology.
M. glareolus as a model system in Ireland
In Ireland, the bank vole presents a unique opportunity as a model system. It has a verifiable introduction point in Foynes, Co. Limerick, has been shown to spread by about 2.5 km per year, and has no current eradication plan. Previous studies by Loxton et al. (2016; 2017) and Stuart et al. have studied the parasite species present in the bank vole and wood mouse in Ireland, with the bank vole harbouring fewer parasite species, resulting in “enemy release” (i.e. the introduced bank vole is relatively free of parasitic burden compared to native competitors).
Stuart et al. explicitly demonstrated that the bank vole exhibits enemy release within Ireland, with bank voles at the expansion front were less parasitised compared to their conspecifics in core populations. The bank vole has also caused a dilution effect for the native wood mouse, with the wood mouse showing lower parasite species abundance at the invasion core, compared to populations at the expansion front and in uninvaded sites. Despite this, the wood mouse also showed increased abundances of the nematode worms Syphacia stroma and S. lobata, suggesting while parasite density may be lower overall, some parasite species are taking advantage of this to increase in their native host population.
The bank vole currently occupies about 40% of the island and continues to expand its range. Accompanied by the presence of baseline knowledge and data, as a model system, the bank vole invasion provides the opportunity to further investigate how parasite communities change as the bank vole becomes more established. The presence of uninvaded sites in the Stuart et al. study provides the opportunity to investigate the early changes that occur when the invader first enters the ecosystem.
The addition of a second invader, the greater white-toothed shrew (Crocidura russula), has also presented another avenue to explore, (as shown by Montgomery, Lundy and Reid), it has a positive synergistic effect on bank vole numbers, while causing a negative effect on the wood mouse numbers and local perturbation of the native pygmy shrew (Sorex minutus).
As demonstrated by international studies, wild rodents, due to their ecology and biology, prove to be good model systems for studying disease in wildlife. Likewise, longitudinal studies on the bank vole invasion have the potential to offer key insights into studying disease and ecoimmunology during a biological invasion, with the potential to give a key insight to the changes in pathogen dynamics during the early stages of the invasion.
Ongoing work utilising this model system.
While the paper outlines the need for continuing research into the bank vole model, this has already begun at Munster Technological University with my supervisor Dr. Peter Stuart. Fieldwork has been completed for the spring and autumn seasons with gut dissections well underway to detect the parasites present. Alongside this, our partners in the BioRodDis group are analysing samples we have sent to detect various bacteria and viruses present in Irish rodents, along with samples from around Europe, helping to make a large database of the rodent pathogens present.