Public awareness and perception of zoonoses has dramatically increased in the last few months due to COVID-19. We invited Drs. Christian Imholt and Anna Obiegala, expert disease ecologists, to explain their perspectives on the emergence of zoonotic diseases in the context of human interference and habitat disturbance.

Christian Imholt¹ & Anna Obiegala²

¹ Julius Kühn-Institute, Federal Research Institute for Cultivated Plants, Institute for Plant Protection in Horticulture and Forests, Vertebrate Research, Münster, Germany

² Institute of Animal Hygiene and Veterinary Public Health, University of Leipzig, Leipzig, Germany

In the present age of COVID-19 it is not surprising that the relationship between biodiversity and the emergence of zoonotic diseases has made it to the prime-time news and political talk shows. However, the causal mechanisms of the relationship between biodiversity and zoonotic diseases are still at the centre of a lively debate (Yingying Wang has summed this up in her post from April). In general, changes in species composition can lead to epidemiological changes of a focal pathogen depending on the ratio, abundance and interaction of competent (amplifying) and non-competent (diluting) hosts. So, in any given system we can expect that the overall community competence is a net result of both dilution and amplification.   

Even with an ongoing, healthy debate on the generality of biodiversity-disease relationships, there is compelling evidence to  promote the conservation of our natural heritage in order to mitigate human health impacts from zoonoses in a Win-Win situation. Despite the overall improvement in health services over the last century, a dramatic increase in the spread of infectious diseases has been observed globally in the last decades, most notably Ebola viruses, HI viruses, Hanta viruses, West Nile virus, MERS-CoV and SARS-CoV-1 and 2. Many factors have been suggested to drive this phenomenon (incl. globalized travel and trade), but the most dominant one seems to be habitat degradation and the associated loss of biodiversity.

Human encroachment on natural resources inevitably leads to increased contact among wildlife, livestock and humans, and increases the probability of host-switching of novel and emerging zoonotic pathogens from various mammalian sources (Mollentze et al., 2020). However, in increasingly disturbed landscapes, vertebrate communities are mainly dominated by generalist species (McFarlane et al., 2012) as most drivers of biodiversity loss (urbanization, habitat fragmentation and agricultural intensification) favor species traits like high reproductive potential, flexible social systems and high dispersal abilities. Such species belong mostly to the order Rodentia. In that order, the species most resilient to human disturbance also carry a higher proportion of zoonotic pathogens (Palma et al., 2012). These species are also more likely to facilitate host-switching to humans or livestock given their tolerance towards human activity (Bordes et al., 2017).

There is a pervasive dialectic in the perception of rodents in the public eye as well as in the scientific literature. Their reproductive potential allows for high amplitude eruptive population fluctuations (generally termed “outbreaks”) in some species. On the one hand, these species can have a multifaceted influence on ecosystem services (predator diversity (Hanski et al., 1995); soil structure and nutrient fluxes (Platt et al., 1996); seed dispersal (Bricker et al., 2010)). On the other hand, they lead to enormous damage during outbreaks, and to monetary losses in agriculture (Jacob & Tkadlec, 2010). Moreover, in many parts of the world, rodents are a major threat to food security (Stenseth et al., 2003).

More relevant in the current situation is the diversity of pathogens harboured by rodents (Meerburg et al., 2009) and their relevance for human health. For example, high amplitude outbreaks of many wild and synanthropic (living in close association with humans) species are associated with human infection risk of zoonotic pathogens. In sub-Saharan Africa, outbreaks of Mastomys spp. cause high damage to crops and transmit the Lassa virus to humans, while in the urban environment the Norway rat (Rattus norvegicus) is the main reservoir for Leptospira spp. causing leptospirosis, one of the most important and widespread zoonotic diseases, in humans and livestock. In a European context, the Puumala orthohantavirus, transmitted by the bank vole (Clethrionomys glareolus) is one of the most widespread zoonotic pathogens (Reil et al., 2017). In addition, ticks and tick-borne pathogens heavily rely on rodents to complete their life-cycle. In central Europe the most common tick species is the castor bean tick (Ixodes ricinus). Due to the wide spectrum of hosts and environmental plasticity, I. ricinus (Gervasi et al. 2015) is the main vector for most zoonotic tick-borne diseases, like Lyme borreliosis. It is assumed that tick populations and tick-borne diseases may be expanding in future. Climate change is frequently invoked as a cause of expansions in incidence rates of Lyme disease but also for other tick-borne diseases such as tick-borne encephalitis, granulocytic anaplasmosis and babesiosis (Ostfeld et al. 2015).

There are strong synergies between zoonotic disease and pest management as both have undergone a simultaneous shift in paradigm in the past decades. Prior to the 1980s, pest management heavily relied on chemical compounds, but increasing development of resistance to those compounds and overall environmental concern have led to the development of alternative management methods. Ecologically-based rodent management focuses on understanding ecological drivers of population dynamics and ecosystem services to devise management options. Similarly, the implementation of the One Health initiative recognizes the interdependence among environmental, human and animal health. However, rodents and vectors of rodent-associated pathogens tend to evade a global one-fits-all management solution given their overall diversity and adaptiveness. There is a large toolbox of management options available but they have to be tailored to manage the focal species or pathogen. Considerable advancements are predictive tools based on environmental variables. These have successfully been applied to species in sub-Saharan Africa (Leirs et al., 1996) as well as to house mice in Australia (Pech et al., 1999). In Germany, a similar model has been developed to predict outbreaks of the bank vole (Imholt et al., 2015), which is used to alert health officials and risk groups in endemic hantavirus regions (Binder et al., 2019). All these efforts rely on an intricate knowledge of the mechanistic cascade from environmental drivers to rodent-pathogen dynamics to crop damage and human infection risk.

Long-term functional biodiversity research presents an ideal opportunity to investigate these specific relationships in order to stack the toolbox of rodent/disease management, but this has rarely been performed. In an ongoing project (shameless self-plug afoot) as part of the Biodiversity Exploratories in Germany (www.biodiversity-exploratories.de) we are assessing how subtle gradients in land-use practices (Mowing, Grazing, Fertilization) can impact the transmission of multi-host mammalian as well as vector-borne pathogens (https://www.researchgate.net/project/Land-use-Biodiversity-and-Rodent-borne-diseases-LaBiRo). The identification of certain land-use practices that might dilute or amplify disease transmission depending on pathogen traits could help to devise suitable management option for farmers and other stakeholders to manage rodents/ vectors and pathogens. After all, the goal is not to eradicate rodents, but to achieve an environmental and socioeconomic balance with human interests.

Related content from Functional Ecology and the British Ecological Society

• Functional Ecology’ Special Feature: Invasions and Infections
• Kate Jones’s Ecology Live! talk – How Bats Changed the World
• Phylogenetic structure of wildlife assemblages shapes patterns of infectious livestock diseases in Africa – Wang et al. Winner of Functional Ecology’s Haldane Prize for Early Career Research!
• The BES Parasite and Pathogen Ecology and Evolution Special Interest Group.
• Yingying Wang’s blogpost on her research into patterns of infectious diseases

References

Binder, F., Drewes, S., Imholt, C., Saathoff, M., Below, D. A., Bendl, E., … Brockmann, S. (2019). Heterogeneous Puumala orthohantavirus situation in endemic regions in Germany in summer 2019. Transboundary and Emerging Diseases, 67(2), 502-509.

Bordes, F., Caron, A., Blasdell, K., de Garine-Wichatitsky, M., & Morand, S. (2017). Forecasting potential emergence of zoonotic diseases in South-East Asia: network analysis identifies key rodent hosts. Journal of Applied Ecology, 54(3), 691–700.

Bricker, M., Pearson, D., & Maron, J. (2010). Small-mammal seed predation limits the recruitment and abundance of two perennial grassland forbs. Ecology, 91(1), 85–92. doi: 10.1890/08-1773.1

Gervasi, S. S., Civitello, D. J., Kilvitis, H. J., & Martin, L. B. (2015). The context of host competence: a role for plasticity in host–parasite dynamics. Trends in Parasitology, 31(9), 419–425.

Hanski, I., Hansson, L., & Henttonen, H. (1991). Specialist Predators, Generalist Predators, and the Microtine Rodent Cycle. Journal of Animal Ecology, 60(1), 353–367. doi: 10.2307/5465

Imholt, C., Reil, D., Eccard, J. A., Jacob, D., Hempelmann, N., & Jacob, J. (2015). Quantifying the past and future impact of climate on outbreak patterns of bank voles (Myodes glareolus). Pest Management Science, 71(2), 166–172. doi: 10.1002/ps.3838

Jacob, J., & Tkadlec, E. (2010). Rodent Outbreaks: Ecology and Impacts. Int. Rice Res. Inst.

Leirs, H., Verhagen, R., Verheyen, W., Mwanjabe, P., & Mbise, T. (1996). Forecasting rodent outbreaks in Africa: an ecological basis for Mastomys control in Tanzania. Journal of Applied Ecology, 937–943.

McFarlane, R., Sleigh, A., & McMichael, T. (2012). Synanthropy of Wild Mammals as a Determinant of Emerging Infectious Diseases in the Asian-Australasian Region. Ecohealth, 9(1), 24–35. doi: 10.1007/s10393-012-0763-9

Meerburg, B. G., Singleton, G. R., & Kijlstra, A. (2009). Rodent-borne diseases and their risks for public health. Critical Reviews in Microbiology, 35(3), 221–270. doi: 10.1080/10408410902989837

Mollentze, N., & Streicker, D. G. (2020). Viral zoonotic risk is homogenous among taxonomic orders of mammalian and avian reservoir hosts. Proceedings of the National Academy of Sciences, 117(17), 9423–9430.

Ostfeld, R. S., & Brunner, J. L. (2015). Climate change and Ixodes tick-borne diseases of humans. Philosophical Transactions of the Royal Society B: Biological Sciences, 370(1665).

Palma, R. E., Polop, J. J., Owen, R. D., & Mills, J. N. (2012). Ecology of Rodent-Associated Hantaviruses in the Southern Cone of South America: Argentina, Chile, Paraguay, and Uruguay. Journal of Wildlife Diseases, 48(2), 267–281. doi: 10.7589/0090-3558-48.2.267

Pech, R. P., Hood, G. M., Singleton, G. R., Salmon, E., Forrester, R. I., & Brown, P. R. (1999). Models for predicting plagues of house mice (Mus domesticus) in Australia. Ecologically-Based Management of Rodent Pests’.(Eds GR Singleton, LA Hinds, H. Leirs and Z. Zhang.) Pp, 81–112.

Platt, B. F., Kolb, D. J., Kunhardt, C. G., Milo, S. P., & New, L. G. (2016). Burrowing Through the Literature: The Impact of Soil-Disturbing Vertebrates on Physical and Chemical Properties of Soil. Soil Science, 181(3–4), 175–191. doi: 10.1097/SS.0000000000000150

Reil, D., Rosenfeld, U. M., Imholt, C., Schmidt, S., Ulrich, R. G., Eccard, J. A., & Jacob, J. (2017). Puumala hantavirus infections in bank vole populations: host and virus dynamics in Central Europe. Bmc Ecology, 17, 9. doi: 10.1186/s12898-017-0118-z

Stenseth, N. C., Leirs, H., Skonhoft, A., Davis, S. A., Pech, R. P., Andreassen, H. P., … Wan, X. R. (2003). Mice, rats, and people: the bio-economics of agricultural rodent pests. Frontiers in Ecology and the Environment, 1(7), 367–375. doi: 10.1890/1540-9295(2003)001[0367:MRAPTB]2.0.CO;2