Infection in dynamic social networks of a wild mammal

Lead Research Organisation: University of Exeter
Department Name: Biosciences

Abstract

The ways in which humans transmit infections depend on the nature of the pathogen and how individuals contact one another. Some individuals, who are particularly well connected, might expect to receive and spread infection frequently, while others that are socially isolated might be expected to avoid general epidemics. In practice, human populations are usually divided into social cliques, around families, schools and workplaces, where interaction is more intense, set against a background of looser connections. Such variable patterns of interaction can be mapped into a social network, where the characteristics of individuals might relate to their risks of being infected and of being a source of infection.

Human social networks and their association with infection are quite well understood, particularly for childhood infections, such as measles, and sexually transmitted diseases, such as HIV. The same is not true of wild animals, where we still tend to think in population terms, of individuals being uniform and having simple social lives. Social networks of infection have been studied in a few wildlife species, including Tasmanian devils, meerkats and giraffes. In one or two cases, including our pilot studies of badgers, the network positions of individuals have been shown to relate to the presence of infection. However, it is hard to know which came first, the infection or the position? Did animals catch infection because they were leading risky lives, were stressed or had reduced immunity? Or were they putting their resources into reproduction instead of fighting infections and so enhancing their lifetime fitness? Did the infection itself affect their behaviour? Or did they occupy this position because they were infected, perhaps because they were ostracised by other members of their social group?

Given that many important infections of humans and livestock, such as influenza viruses, originate from wild animals, it would be useful to understand how to manage such emerging infections in wildlife. Badgers are a good example. Because they are a reservoir of bovine tuberculosis (TB), which can affect a range of mammals including cattle and humans, they are often culled in an attempt to control the disease. They are also hosts for rabies and U.K. rabies contingency plans currently provide for badgers to be culled to protect human health. The current pilot badger culls being conducted in England are a test of whether effective culling can be implemented by the farming industry, in the hope that this might control TB infection in cattle. Unexpectedly, it has been shown in earlier trials that culling badgers can also bring about increases in new cases of TB in badgers, and in cattle. This has been hypothesised to stem from a "perturbation effect", whereby culling upsets the otherwise stable social behaviour of badgers, causing them to roam, and transmit infection, more widely. Despite the prominence of the badger TB problem and widespread awareness of this "perturbation effect", we know surprisingly little about how infection is transmitted between badgers and how this is affected by culling. This project will look in detail at infection in wild animal networks, using badgers as an example, paying particular attention to social behaviour and individual condition, and working out what these mean for disease control.

We are proposing to use intensively monitored populations of wild badgers to study a range of "indicator" infections and how they relate to behaviour, stress, immune function, reproductive activity and success. Our work will give us an understanding of how infections spread, or do not spread, across real networks and will help improve understanding of the "perturbation effect". Then we will build a computer model of infections in our observed networks and use the model to test strategies to determine which is best for disease control, for badgers and TB, and for animal diseases more generally.

Planned Impact

Bovine tuberculosis is probably the greatest challenge in animal health policy and practice in the U.K. and has a large and increasing economic and social impact. Because of the involvement of badgers, policy in this area has become fraught with difficulty and conflict among ardent stakeholder groups. It looks likely that the disease problem will continue to worsen, while conflict around badger management intensifies. Badger ecology, social behaviour and the "perturbation effect" have been shown to be critical, in both biological and policy terms, for transmission and control of TB.

More generally, a high proportion of emerging infections of humans are zoonotic in origin and so the control of infection in wildlife hosts is becoming more important to the protection of human and animal health. Therefore, while we expect this work to be of particular benefit to TB control, it will also make a significant and general contribution to wildlife disease control internationally.

Animal health officials in government departments and agencies.
Bovine TB costs British taxpayers ~£100M p.a. and resulted in the slaughter of ~37,000 cattle in GB in 2012. Control is a high priority for Ministers in Defra, Welsh Government and Northern Ireland Executive; Each of these administrations is adopting its distinct policy for disease control in cattle and wildlife. Defra is contemplating badger culling across large parts of western England. If generalised, proactive culling (as is being piloted) is not adopted, Defra ministers have identified more targeted culling, perhaps in combination with vaccination, as a potential policy option. Wales is focusing on vaccination, while in Northern Ireland, policy is focused on targeted removal or vaccination. The economic impact assessment that underpins Defra current policy, the licensing decisions made by Natural England and the statutory advice given by the Chief Veterinary Officer, all draw heavily on understanding of badger social behaviour, and perturbation in particular. Knowledge gained from this study will contribute to policy development on all these fronts because understanding of badger behaviour, perturbation and its outcomes is critical to all options for badger management.

Veterinarians, farmers, conservationists, animal welfare scientists.
Representative organisations, campaign groups and their publics.
Badger management is a topic of controversy and active social debate. Those who frame this debate frequently draw on their knowledge of badger social structure, perturbation, its effects and mitigation, but do so in a very broad and narrative way. The "perturbation effect" as a concept has achieved remarkably widespread public understanding, extending beyond academic work and permeating into popular media and public consciousness so that it underpins general knowledge of the badger-TB problem. To inform key actors in this debate, our project will help explain the importance of badger social behaviour, the perturbation effect, how it works and what its consequences are.

Disease control specialists internationally.
Globally, a high proportion of emerging infections arise from wildlife. Hence the control of the spread of infection in wild animal hosts is of key strategic relevance to protection of human and livestock health. Furthermore, infection has emerged as an important factor threatening conservation of biodiversity. Since counter-productive and counter-intuitive outcomes of wildlife control have been observed in relation to control of rabies in bats and foxes, spongiform encephalopathy in deer and swine fever in boar, amongst others, the consequences of culling for social systems and disease transmission in wildlife is likely to be manifest. By building on investigations of a well-studied system, this project will inform the direction of wildlife management for disease control more widely.

Publications

10 25 50
publication icon
Silk MJ (2018) Can Multilayer Networks Advance Animal Behavior Research? in Trends in ecology & evolution

publication icon
Silk MJ (2019) Integrating social behaviour, demography and disease dynamics in network models: applications to disease management in declining wildlife populations. in Philosophical transactions of the Royal Society of London. Series B, Biological sciences

publication icon
Silk M (2017) The application of statistical network models in disease research in Methods in Ecology and Evolution

 
Description This work has underlined the importance of social structure for the transmission and control of infectious diseases in wild animals. By analysing long term data, using modelling and conducting experiments, we have improved understanding of how social structure varies among individuals, types of animal and with time. We then used this information to understand how disease spreads and might be controlled. The work is of particular relevance to the UK because of the role of badgers in the maintenance and transmission of bovine tuberculosis (bTB) in cattle, which is a major economic, animal health and social problem in this country. Our work has contributed to fundamental understanding of the epidemiology of bTB in wildlife and extends to potential control measures for this important infection.
Exploitation Route Bovine tuberculosis is a major social, political and environmental challenge for the UK. This work contributes fundamental understanding of bTB epidemiology in the major wildlife host. The project has also led to a Knowledge Exchange Fellowship, supported by NERC, that supports and improves sharing of fundamental and applied science with user communities, specifically regional TB eradication groups.
Sectors Agriculture, Food and Drink

 
Description Our research has supported regional TB eradication groups, including via a related Knowledge Exchange fellowship.
First Year Of Impact 2017
Sector Agriculture, Food and Drink
Impact Types Societal,Policy & public services

 
Description Support for regional TB eradication groups
Geographic Reach Local/Municipal/Regional 
Policy Influence Type Membership of a guideline committee
Impact The Principal Investigator is a member and vice-chair of the Cornwall TB Eradication Group, which comprises farmers, vets, regulators and scientists, and serves to accelerate progress towards eradication of bTB from cattle in Cornwall and the wider UK. Regular contributions to this group focus on badger ecology, bTB epidemiology and draw on the findings of this project.
URL http://www.cornwalltbeg.co.uk
 
Description Efficient Bayesian modelling of infectious diseases in wildlife
Amount £321,242 (GBP)
Funding ID NE/V000616/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 08/2020 
End 08/2022
 
Description Industrial Strategy CASE studentships via DTP
Amount £85,000 (GBP)
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 09/2017 
End 03/2021
 
Description Open Knowledge Exchange Fellowships
Amount £147,890 (GBP)
Funding ID NE/P006396/1 
Organisation Natural Environment Research Council 
Sector Public
Country United Kingdom
Start 04/2017 
End 03/2020
 
Title Geolocated proximity logging 
Description We have developed a tag that records where contact events among wild animals take place. 
Type Of Material Physiological assessment or outcome measure 
Provided To Others? No  
Impact This technique will allow us to describe spatial and temporal dynamics in animal social networks. 
 
Title CMRNet 
Description Long-term capture-mark-recapture data provide valuable information on the movements of individuals between locations, and the contemporary and/or co-located captures of individuals can be used to approximate the social structure of populations. We introduce an r package (CMRnet) that generates social and movement networks from spatially explicit capture-mark-recapture data. It also provides functions for network and datastream permutations for these networks. Here we describe the package and key considerations for its application, providing two example case studies. The conversion of spatially explicit mark-recapture data into social and movement networks will provide insights into the interplay between demography and behaviour in wild animal populations, with important applications in their management and conservation. 
Type Of Material Data analysis technique 
Year Produced 2020 
Provided To Others? Yes  
Impact Ongoing 
URL https://doi.org/10.1111/2041-210X.13502
 
Title Genetic evidence further elucidates the history and extent of badger introductions from Great Britain into Ireland 
Description The colonization of Ireland by mammals, has been the subject of extensive study using genetic methods, and forms a central problem in understanding the phylo-geography of European mammals after the Last Glacial Maximum. Ireland exhibits a de-pauperate mammal fauna relative to Great Britain and continental Europe, and a range of natural and anthropogenic processes have given rise to its modern fauna. Previous Europe-wide surveys of the European badger (Meles meles) have found conflicting microsatellite and mitochondrial DNA evidence in Irish populations, suggesting Irish badgers have arisen from a combination of populations with close relationships in Great Britain and in Scandinavia, and admixture between recently introduced and longer established populations. The extent and history of contact between British and Irish badger populations, however, remains unclear. We use comprehensive genetic data from Great Britain and Ireland to demonstrate that badgers in Ireland's northeastern and southeastern counties are genetically similar to contemporary British populations. Simulation analyses suggest this admixed population arose in Ireland 600-700 (CI 100-2600) years before present most likely through introduction of British badgers by people. These findings add to our knowledge of the complex colonization history of Ireland by mammals, and the central role of humans in facilitating it. 
Type Of Material Database/Collection of data 
Year Produced 2019 
Provided To Others? Yes  
URL http://datadryad.org/stash/dataset/doi:10.5061/dryad.4xgxd2555
 
Title Network data for analysis of wildlife disease (Bioscience) 
Description Data underpinning methodological approaches detailed in Matthew J. Silk, Darren P. Croft, Richard J. Delahay, David J. Hodgson, Mike Boots, Nicola Weber, Robbie A. McDonald; Using Social Network Measures in Wildlife Disease Ecology, Epidemiology, and Management, BioScience, Volume 67, Issue 3, 1 March 2017, Pages 245-257, https://doi.org/10.1093/biosci/biw175 
Type Of Material Database/Collection of data 
Year Produced 2017 
Provided To Others? Yes  
Impact N/A 
URL https://academic.oup.com/bioscience/article/67/3/245/2962460
 
Title Network data for analysis of wildlife disease (Ecology Letters) 
Description Data underpinning network analyses of transmission of infection in wild badgers. As published in Silk MJ, Weber NL, Steward LC, Hodgson DJ, Boots M, Croft DP, Delahay RJ, McDonald RA (2017) Data from: Contact networks structured by sex underpin sex-specific epidemiology of infection. Dryad Digital Repository. , 
Type Of Material Database/Collection of data 
Year Produced 2017 
Provided To Others? Yes  
Impact N/A 
URL https://doi.org/10.5061/dryad.s1502
 
Title Network data for analysis of wildlife disease (Ecology and Evolution) 
Description Data underpinning Silk MJ, Weber N, Steward LC, Delahay RJ, Croft DP, Hodgson DJ, Boots M, McDonald RA (2017) Seasonal variation in daily patterns of social contacts in the European badger Meles meles. Ecology and Evolution 7(21): 9006-9015. https://doi.org/10.1002/ece3.3402 
Type Of Material Database/Collection of data 
Year Produced 2017 
Provided To Others? Yes  
Impact N/A 
URL https://doi.org/10.5061/dryad.jr0s5
 
Title Network data for analysis of wildlife disease (Methods in Ecology and Evolution) 
Description Data underpinning methodological approaches outlined in Silk, M. J., Croft, D. P., Delahay, R. J., Hodgson, D. J., Weber, N., Boots, M., McDonald, R. A. (2017), The application of statistical network models in disease research. Methods in Ecology and Evolution, 8: 1026-1041. doi: 10.1111/2041-210X.12770 
Type Of Material Database/Collection of data 
Year Produced 2017 
Provided To Others? Yes  
Impact N/A 
URL http://onlinelibrary.wiley.com/wol1/doi/10.1111/2041-210X.12770/full
 
Description Wildlife Research Co-operative (University of Exeter and Animal and Plant Health Agency) 
Organisation Animal Health And Veterinary Laboratories Agency (AHVLA)
Country United Kingdom 
Sector Public 
PI Contribution We work closely with the National Wildlife Research Centre of the Animal and Plant Health Agency (formerly AHVLA), including data sharing, combined fieldwork in the field, shared wildlife and scientific procedures licensing. We collaborate further across a range of RCUK studentships, including iCASE awards. We help develop policy relevant science outcomes for use in advice to officials and others.
Collaborator Contribution APHA share data, co-supervise students, deliver fieldwork in partnership, hold statutory licenses.
Impact We have jointly supervised >25 PGR students, published >20 papers since 2012, supported development of policy and practice across a range of topics, primarily related to control of bovine tuberculosis.
Start Year 2007
 
Description TB eradication group TB control meetings 
Form Of Engagement Activity Participation in an activity, workshop or similar
Part Of Official Scheme? No
Geographic Reach Regional
Primary Audience Industry/Business
Results and Impact As part of the activities of the TB Eradication Groups, the PI has participated in local awareness-raising meetings for farmers and vets in relation to TB control.
Year(s) Of Engagement Activity 2017,2018,2019
URL http://www.cornwalltbeg.co.uk