A model-based approach for investigation and mitigation of disease spillover risks to wildlife: Dogs, foxes and canine distemper in central India

Multi-host pathogens can pose a serious conservation threat when free-ranging domestic animal populations occur alongside susceptible populations of wild species. An example is canine distemper virus (CDV), which can occur at high prevalence in domestic dog (Canis familiaris) populations from which it may be transmitted (spillover) into wild carnivore populations. Effective management of such disease threats is hindered by our limited understanding of the the dynamics of interspecific CDV transmission in natural settings. We used a modeling approach to better understand CDV spillover threats to wild Indian foxes (Vulpes bengalensis) occurring in a protected grassland habitat in central India. An agent-based stochastic simulation model was built, and parameterized with data from ecological and epidemiological studies. Based on the sensitivity analyses of the model, the CDV incidence rate in dogs was most influenced by the proportion of roamer dogs in the dog population. The CDV incidence rate in dogs was also sensitive to the CDV introduction frequency in the dog population. The proportion of roamer dogs in the dog population also influenced the number of CDV spillover events. The basic reproductive number (R0) for CDV in the model fox population was 0.85, indicating that CDV could not be independently sustained in the fox population. We used the model to explore potential management strategies to mitigate the risk of CDV spillover. Vaccination of local dog populations was an ineffective disease control strategy, while fox vaccination was highly effective. Interventions potentially resulting in lower contact rates between dogs and foxes, like reduction in village dog density and restricting dog movements in fox habitat, implemented in a sustained and integrated manner would be most effective in mitigating disease threats to foxes. Such modeling approaches can be used to better understand disease threats for other species of management concern, and to contrast potential management interventions.

[1]  Aaron P. Wagner,et al.  Rabies Virus and Canine Distemper Virus in Wild and Domestic Carnivores in Northern Kenya: Are Domestic Dogs the Reservoir? , 2012, EcoHealth.

[2]  M. Laurenson,et al.  Trapping and vaccination of endangered Ethiopian wolves to control an outbreak of rabies , 2007 .

[3]  J. Butler,et al.  Dogs, disease and wildlife , 2014 .

[4]  A. Vanak,et al.  Interference competition at the landscape level: the effect of free-ranging dogs on a native mesocarnivore , 2010 .

[5]  Mark Bartlett,et al.  The Critical Community Size for Measles in the United States , 1960 .

[6]  S. Krakowka,et al.  Age-related susceptibility to infection with canine distemper virus in gnotobiotic dogs. , 1976, The Journal of infectious diseases.

[7]  R. Plowright,et al.  Causal inference in disease ecology: investigating ecological drivers of disease emergence , 2008 .

[8]  M. Gompper,et al.  Seroprevalence of pathogens in domestic carnivores on the border of Madidi National Park, Bolivia , 2004, Animal conservation.

[9]  Chris T Bauch,et al.  Stray dog population demographics in Jodhpur, India following a population control/rabies vaccination program. , 2010, Preventive veterinary medicine.

[10]  S. Cleaveland,et al.  Canine vaccination--providing broader benefits for disease control. , 2006, Veterinary microbiology.

[11]  M. Gompper,et al.  Assessing demographic and epidemiologic parameters of rural dog populations in India during mass vaccination campaigns. , 2013, Preventive veterinary medicine.

[12]  A. Vanak,et al.  Dogs Canis familiaris as carnivores: their role and function in intraguild competition , 2009 .

[13]  N. Barlow.  The ecology of wildlife disease control : simple models revisited , 1996 .

[14]  M. Day,et al.  WSAVA Guidelines for the vaccination of dogs and cats. , 2010, The Journal of small animal practice.

[15]  M. Bush,et al.  Clinical trials with canine distemper vaccines in exotic carnivores. , 1983, Journal of the American Veterinary Medical Association.

[16]  A. Pusey,et al.  Human impacts, disease risk, and population dynamics in the chimpanzees of Gombe National Park, Tanzania , 2008, American journal of primatology.

[17]  S. Kapil,et al.  Canine Distemper Spillover in Domestic Dogs from Urban Wildlife , 2011, Veterinary Clinics of North America: Small Animal Practice.

[18]  D. Saltz,et al.  The impact of free-roaming dogs on gazelle kid/female ratio in a fragmented area , 2004 .

[19]  E. Williams,et al.  Infectious diseases of wild mammals. , 2001 .

[20]  S. Carter,et al.  Serosurvey for canine distemper virus exposure in dogs in communal lands in Zimbabwe. , 2005, Journal of the South African Veterinary Association.

[21]  A. Dobson,et al.  INFECTIOUS DISEASE AND INTENSIVE MANAGEMENT: POPULATION DYNAMICS, THREATENED HOSTS, AND THEIR PARASITES , 1993 .

[22]  Craig Packer,et al.  Distinguishing epidemic waves from disease spillover in a wildlife population , 2009, Proceedings of the Royal Society B: Biological Sciences.

[23]  S. K. Pal.  Population ecology of free-ranging urban dogs in West Bengal, India , 2001, ACTA THERIOLOGICA.

[24]  C. Gortázar,et al.  Carnivore population trends in Spanish agrosystems after the reduction in food availability due to rabbit decline by rabbit haemorrhagic disease and improved waste management , 2009, European Journal of Wildlife Research.

[25]  A. Dobson,et al.  The role of pathogens in biological conservation , 2002 .

[26]  A. Rahmani,et al.  Population and Ecology of the Indian Fox Vulpes Bengalensis At Rollapadu Wildlife Sanctuary, Andhra Pradesh, India , 2000 .

[27]  J. Ellis,et al.  Exposure to infectious agents in dogs in remote coastal British Columbia: Possible sentinels of diseases in wildlife and humans. , 2011, Canadian journal of veterinary research = Revue canadienne de recherche veterinaire.

[28]  S. Cleaveland,et al.  Urban domestic dog populations as a source of canine distemper virus for wild carnivores in the Coquimbo region of Chile. , 2011, Veterinary microbiology.

[29]  J.A.P. Heesterbeek.  A Brief History of R0 and a Recipe for its Calculation , 2002, Acta biotheoretica.

[30]  E. Hiby,et al.  Fecundity and longevity of roaming dogs in Jaipur, India , 2008, BMC veterinary research.

[31]  Gillespie Jh,et al.  Canine Distemper Virus , 1972, Virology Monographs / Die Virusforschung in Einzeldarstellungen.

[32]  R. Woodroffe.  Managing disease threats to wild mammals , 1999 .

[33]  M. Thaker,et al.  Experimental examination of behavioural interactions between free-ranging wild and domestic canids , 2009, Behavioral Ecology and Sociobiology.

[34]  K. Alexander,et al.  AFRICAN WILD DOGS (LYCAON PICTUS) ENDANGERED BY A CANINE DISTEMPER EPIZOOTIC AMONG DOMESTIC DOGS NEAR THE MASAI MARA NATIONAL RESERVE, KENYA , 1994, Journal of wildlife diseases.

[35]  M. G. Garner,et al.  Controlling disease outbreaks in wildlife using limited culling: modelling classical swine fever incursions in wild pigs in Australia , 2012, Veterinary Research.

[36]  K. Goller,et al.  Fatal canine distemper infection in a pack of African wild dogs in the Serengeti ecosystem, Tanzania. , 2010, Veterinary microbiology.

[37]  S. Cleaveland,et al.  Rabies control in rural Africa: evaluating strategies for effective domestic dog vaccination. , 2009, Vaccine.

[38]  Birgit Müller,et al.  A standard protocol for describing individual-based and agent-based models , 2006 .

[39]  L. H. Taylor,et al.  Identifying Reservoirs of Infection: A Conceptual and Practical Challenge , 2002, Emerging infectious diseases.

[40]  M. Laurenson,et al.  RABIES IN AFRICAN WILD DOGS (LYCAON PICTUS) IN THE SERENGETI REGION, TANZANIA , 1993, Journal of wildlife diseases.

[41]  Craig Packer,et al.  Transmission Dynamics and Prospects for the Elimination of Canine Rabies , 2009, PLoS biology.

[42]  J. McDermott,et al.  Dog ecology and demography information to support the planning of rabies control in Machakos District, Kenya. , 2001, Acta tropica.

[43]  P. Cross,et al.  Persistence of canine distemper virus in the Greater Yellowstone ecosystem's carnivore community. , 2010, Ecological applications : a publication of the Ecological Society of America.

[44]  L. Mugisha,et al.  Serosurvey of Dogs for Human, Livestock, and Wildlife Pathogens, Uganda , 2013, Emerging infectious diseases.

[45]  S. Cleaveland,et al.  Demography of domestic dogs in rural and urban areas of the Coquimbo region of Chile and implications for disease transmission. , 2010, Preventive veterinary medicine.

[46]  Andrew P. Dobson,et al.  Microparasite transmission and persistence , 2002 .

[47]  J. Gareth Polhill,et al.  The ODD protocol: A review and first update , 2010, Ecological Modelling.

[48]  M. Gompper,et al.  To vaccinate or not to vaccinate: lessons learned from an experimental mass vaccination of free‐ranging dog populations , 2015 .

[49]  L. Nel,et al.  Rabies in African wild dogs (Lycaon pitus) in the Madikwe Game Reserve, South Africa , 2000, Veterinary Record.

[50]  M. S. Gunther,et al.  An Infectious Disease and Mortality Survey in a Population of Free-Ranging African Wild Dogs and Sympatric Domestic Dogs , 2013 .

[51]  C. Ribble,et al.  Assessing reproductive patterns and disorders in free-ranging dogs in Jodhpur, India to optimize a population control program. , 2010, Theriogenology.

[52]  E. Dubovi,et al.  Serosurvey of Pathogens in Domestic Dogs on the Border of Noël Kempff Mercado National Park, Bolivia , 2008, Journal of zoo and wildlife medicine : official publication of the American Association of Zoo Veterinarians.

[53]  A. Vanak,et al.  Epidemiology of viral pathogens of free-ranging dogs and Indian foxes in a human-dominated landscape in central India. , 2014, Transboundary and emerging diseases.

[54]  F. Martínez,et al.  Management measures to control a feline leukemia virus outbreak in the endangered Iberian lynx , 2009 .

[55]  Yohay Carmel,et al.  Incorporating output variance in local sensitivity analysis for stochastic models , 2008 .