Rabies disease dynamics in naïve dog populations in Australia

Domestic dog roaming patterns in remote northern Australian indigenous communities and implications for disease modelling

Simple SummaryAustralia is historically canine rabies-free but faces the threat of a rabies incursion due to the current spread of rabies through eastern Indonesia. To address this genuine concern, it is necessary to acquire further ecological knowledge on dingo populations in northern Australia to improve our predictions on the potential spread of rabies within dingoes, should an incursion occur. A one-year camera trap study was conducted in northern Australia, where the risk of the introduction of rabies is highest. Our resulting estimates of population density and home range sizes of dingoes in the study area varied according to seasons. Additionally, based on an analysis of spatial use and daily activity patterns from the camera trap pictures, a large spatial correlation and temporal overlap between dingoes and free-roaming community dogs was observed, suggesting a potential risk of disease transmission at the wild–domestic interface. This information will help improve preparedness planning for a rabies incursion in Australia.Australia is currently free of canine rabies. Spatio-ecological knowledge about dingoes in northern Australia is currently a gap that impedes the application of disease spread models and our understanding of the potential transmission of rabies, in the event of an incursion. We therefore conducted a one-year camera trap survey to monitor a dingo population in equatorial northern Australia. The population is contiguous with remote Indigenous communities containing free-roaming dogs, which potentially interact with dingoes. Based on the camera trap data, we derived dingo density and home range size estimates using maximum-likelihood, spatially explicit, mark–resight models, described dingo movements and evaluated spatial correlation and temporal overlap in activities between dingoes and community dogs. Dingo density estimates varied from 0.135 animals/km2 (95% CI = 0.127–0.144) during the dry season to 0.147 animals/km2 (95% CI = 0.135–0.159) during the wet season. The 95% bivariate Normal home range sizes were highly variable throughout the year (7.95–29.40 km2). Spatial use and daily activity patterns of dingoes and free-roaming community dogs, grouped over ~3 month periods, showed substantial temporal activity overlap and spatial correlation, highlighting the potential risk of disease transmission at the wild–domestic interface in an area of biosecurity risk in equatorial northern Australia. Our results have utility for improving preparedness against a potential rabies incursion.

Free-roaming dogs (Canis lupus familiaris) are of public health and conservation concern because of their potential to transmit diseases, such as rabies, to both people and wildlife. Understanding domestic dog population dynamics and how they could potentially be impacted by interventions, such as rabies vaccination, is vital for such disease control efforts. For four years, we measured demographic data on 2,649 free-roaming domestic dogs in four rural villages in Tanzania: two villages with and two without a rabies vaccination campaign. We examined the effects of body condition, sex, age and village on survivorship and reproduction. Furthermore, we compared sources of mortality among villages. We found that adult dogs (>12mos) had higher survival than puppies in all villages. We observed a male-biased sex ratio across all age classes. Overall survival in one non-vaccination village was lower than in the other three villages, all of which had similar survival probabilities. In all villages, dogs in poor body condition had lower survival than dogs in ideal body condition. Sickness and spotted hyena (Crocuta crocuta) predation were the two main causes of dog death. Within vaccination villages, vaccinated dogs had higher survivorship than unvaccinated dogs. Dog population growth, however, was similar in all the villages suggesting village characteristics and ownership practices likely have a greater impact on overall dog population dynamics than vaccination. Free-roaming domestic dogs in rural communities exist in the context of their human owners as well as the surrounding wildlife. Our results did not reveal a clear effect of vaccination programs on domestic dog population dynamics. An investigation of the role of dogs and their care within these communities could provide additional insight for planning and implementing rabies control measures such as mass dog vaccination.

Information on contacts between individuals within a population is crucial to inform disease control strategies, via parameterisation of disease spread models. In this study we investigated the use of dog-borne video cameras–in conjunction with global positioning systems (GPS) loggers–to both characterise dog-to-dog contacts and to estimate contact rates. We customized miniaturised video cameras, enclosed within 3D-printed plastic cases, and attached these to nylon dog collars. Using two 3400 mAh NCR lithium Li-ion batteries, cameras could record a maximum of 22 hr of continuous video footage. Together with a GPS logger, collars were attached to six free roaming domestic dogs (FRDDs) in two remote Indigenous communities in northern Australia. We recorded a total of 97 hr of video footage, ranging from 4.5 to 22 hr (mean 19.1) per dog, and observed a wide range of social behaviours. The majority (69%) of all observed interactions between community dogs involved direct physical contact. Direct contact behaviours included sniffing, licking, mouthing and play fighting. No contacts appeared to be aggressive, however multiple teeth baring incidents were observed during play fights. We identified a total of 153 contacts–equating to 8 to 147 contacts per dog per 24 hr–from the videos of the five dogs with camera data that could be analysed. These contacts were attributed to 42 unique dogs (range 1 to 19 per video) which could be identified (based on colour patterns and markings). Most dog activity was observed in urban (houses and roads) environments, but contacts were more common in bushland and beach environments. A variety of foraging behaviours were observed, included scavenging through rubbish and rolling on dead animal carcasses. Identified food consumed included chicken, raw bones, animal carcasses, rubbish, grass and cheese. For characterising contacts between FRDD, several benefits of analysing videos compared to GPS fixes alone were identified in this study, including visualisation of the nature of the contact between two dogs; and inclusion of a greater number of dogs in the study (which do not need to be wearing video or GPS collars). Some limitations identified included visualisation of contacts only during daylight hours; the camera lens being obscured on occasion by the dog’s mandible or the dog resting on the camera; an insufficiently wide viewing angle (36°); battery life and robustness of the deployments; high costs of the deployment; and analysis of large volumes of often unsteady video footage. This study demonstrates that dog-borne video cameras, are a feasible technology for estimating and characterising contacts between FRDDs. Modifying camera specifications and developing new analytical methods will improve applicability of this technology for monitoring FRDD populations, providing insights into dog-to-dog contacts and therefore how disease might spread within these populations.

Free-roaming dogs (Canis familiaris) are common worldwide, often maintaining diseases of domestic pets and wildlife. Management of these dogs is difficult and often involves capture, treatment, neutering and release. Information on the effects of sex and reproductive state on intraspecific contacts and disease transmission is currently lacking, but is vital to improving strategic management of their populations. We assessed the effects of sex and reproductive state on short-term activity patterns and contact rates of free-roaming dogs living in an Australian Indigenous community. Population, social group sizes and rates of contact were estimated from structured observations along walked transects. Simultaneously, GPS telemetry collars were used to track dogs' movements and to quantify the frequency of contacts between individual animals. We estimated that the community's dog population was 326±52, with only 9.8±2.5% confined to a house yard. Short-term activity ranges of dogs varied from 9.2 to 133.7 ha, with males ranging over significantly larger areas than females. Contacts between two or more dogs occurred frequently, with entire females and neutered males accumulating significantly more contacts than spayed females or entire males. This indicates that sex and reproductive status are potentially important to epidemiology, but the effect of these differential contact rates on disease transmission requires further investigation. The observed combination of unrestrained dogs and high contact rates suggest that contagious disease would likely spread rapidly through the population. Pro-active management of dog populations and targeted education programs could help reduce the risks associated with disease spread.

The wildlife-domestic interface is a key concept helping us to understand how diseases affect both wild and domestic animal populations, yet how to define and measure it remains a challenge. One tool which can contribute to our understanding of the wildlife-domestic interface is disease spread modelling. This can provide insight into how diseases spread within and between populations, and guide decision-making for disease control, response and surveillance programs. Specifically, quantitative estimation of contact rates permits such disease spread models to be developed and used confidently. Here we present a case study of the potential spread of rabies (an exotic disease in Australia) within the wild dog-domestic dog (Canis familiaris) ecosystem of northern Australia to illustrate the concept of the wildlife-domestic interface and disease transmission. We summarise a decade of research conducted to understand one such interface, the wild-domestic dog interface at one site in northern Australia, for the purposes of exploring the impact of one specific disease, rabies. Over a period of 10 years, free-roaming domestic dogs and wild dogs in the Northern Peninsula Area (NPA) of Cape York, Queensland were studied. Key findings included identification of a small but important group of domestic dogs which regularly roam in bushland areas; peri-urban wild dog activity, particularly in the dry season, likely driven by the availability of food sources; and the potential for interaction between hunting dogs and wild dogs in remote areas, particularly during the wet season. These observations can be used to inform disease spread models and identify strategies to mitigate the risks of disease transmission. However, the collection and incorporation of data into such models needs more consideration regarding what information is usable (such as contact rates) and the best ways to collect it. The scarcity of such models incorporating the wildlife-domestic interface suggests that integrated epidemiological-ecological studies are needed to fill this gap.

Potential for transmission of zoonotic helminth infections among dingoes and dogs in the Wet Tropics of North Queensland, Australia

A review of the interactions between free-roaming domestic dogs and wildlife

BackgroundRabies is a serious yet neglected public health threat in resource-limited communities in Africa, where the virus is maintained in populations of owned, free-roaming domestic dogs. Rabies elimination can be achieved through the mass vaccination of dogs, but maintaining the critical threshold of vaccination coverage for herd immunity in these populations is hampered by their rapid turnover. Knowledge of the population dynamics of free-roaming dog populations can inform effective planning and implementation of mass dog vaccination campaigns to control rabies.Methodology/Principal FindingsWe implemented a health and demographic surveillance system in dogs that monitored the entire owned dog population within a defined geographic area in a community in Mpumalanga Province, South Africa. We quantified demographic rates over a 24-month period, from 1st January 2012 through 1st January 2014, and assessed their implications for rabies control by simulating the decline in vaccination coverage over time. During this period, the population declined by 10%. Annual population growth rates were +18.6% in 2012 and -24.5% in 2013. Crude annual birth rates (per 1,000 dog-years of observation) were 451 in 2012 and 313 in 2013. Crude annual death rates were 406 in 2012 and 568 in 2013. Females suffered a significantly higher mortality rate in 2013 than males (mortality rate ratio [MRR] = 1.54, 95% CI = 1.28–1.85). In the age class 0–3 months, the mortality rate of dogs vaccinated against rabies was significantly lower than that of unvaccinated dogs (2012: MRR = 0.11, 95% CI = 0.05–0.21; 2013: MRR = 0.31, 95% CI = 0.11–0.69). The results of the simulation showed that achieving a 70% vaccination coverage during annual campaigns would maintain coverage above the critical threshold for at least 12 months.Conclusions and SignificanceOur findings provide an evidence base for the World Health Organization’s empirically-derived target of 70% vaccination coverage during annual campaigns. Achieving this will be effective even in highly dynamic populations with extremely high growth rates and rapid turnover. This increases confidence in the feasibility of dog rabies elimination in Africa through mass vaccination.

If they could choose: How would dogs spend their days? Activity patterns in four populations of domestic dogs

In many regions of the world domestic dogs are free roaming and live in close relationship with humans. These free-roaming domestic dogs (FRDD) can cause public health problems such as dog bites and transmission of infectious diseases. To effectively control diseases transmitted by FRDD, knowledge on the dogs' behaviour is required. To identify predictors of home range (HR) size, we collected global positioning system data from 135 FRDD living in eight Aboriginal and Torres Strait Islander communities in Northern Australia. The core HR size ranged from 0·17 to 2·33 ha and the extended HR size from 0·86 to 40·46 ha. Using a linear mixed effect model with a Restricted Maximum Likelihood approach, the dog's sex and reproductive status were identified as predictors of roaming. Non-castrated males had the largest HRs, followed by neutered females. Also, FRDDs were found to roam further during the pre- than the post-wet season. These findings have implications for infectious disease spread. Identification of risk groups for disease spread within a population allows for more targeted disease response and surveillance. Further investigation of predictors of roaming in other FRDD populations worldwide would increase the external validity of such studies.

Free roaming domestic dogs (FRDD) are the main vectors for rabies transmission to humans worldwide. To eradicate rabies from a dog population, current recommendations focus on random vaccination with at least 70% coverage. Studies suggest that targeting high-risk subpopulations could reduce the required vaccination coverage, and increase the likelihood of success of elimination campaigns. The centrality of a dog in a contact network can be used as a measure of its potential contribution to disease transmission. Our objectives were to investigate social networks of FRDD in eleven study sites in Chad, Guatemala, Indonesia and Uganda, and to identify characteristics of dogs, and their owners, associated with their centrality in the networks. In all study sites, networks had small-world properties and right-skewed degree distributions, suggesting that vaccinating highly connected dogs would be more effective than random vaccination. Dogs were more connected in rural than urban settings, and the likelihood of contacts was negatively correlated with the distance between dogs’ households. While heterogeneity in dog's connectedness was observed in all networks, factors predicting centrality and likelihood of contacts varied across networks and countries. We therefore hypothesize that the investigated dog and owner characteristics resulted in different contact patterns depending on the social, cultural and economic context. We suggest to invest into understanding of the sociocultural structures impacting dog ownership and thus driving dog ecology, a requirement to assess the potential of targeted vaccination in dog populations.

Controlling and eliminating zoonotic pathogens such as rabies virus, Echinococcus granulosus, and Leishmania spp. require quantitative knowledge of dog populations. Dog population estimates are fundamental for planning, implementing, and evaluating public health programs. However, dog population estimation is time-consuming, requires many field personnel, may be inaccurate and unreliable, and is not without danger. Our objective was to evaluate a remote method for estimating the population of free-roaming dogs using Google Street View (GSV). Adopting a citizen science approach, participants from Arequipa and other regions in Peru were recruited using social media and trained to use GSV to identify and count free-roaming dogs in 20 urban and 6 periurban communities. We used correlation metrics and negative binomial models to compare the counts of dogs identified in the GSV imagery with accurate counts of free-roaming owned dogs estimated via door-to-door (D2D) survey conducted in 2016. Citizen scientists detected 862 dogs using GSV. After adjusting by the proportion of streets that were scanned with GSV we estimated 1,022 free-roaming dogs, while the 2016 D2D survey estimated 1,536 owned free-roaming dogs across those 26 communities. We detected a strong positive correlation between the number of dogs detected by the two methods in the urban communities (r = 0.85; p < 0.001) and a weak correlation in periurban areas (r = 0.36; p = 0.478). Our multivariable model indicated that for each additional free-roaming dog estimated using GSV, the expected number of owned free-roaming dogs decreased by 2% in urban areas (p < 0.001) and increased by 2% in peri-urban areas (p = 0.004). The type of community (urban vs periurban) had an effect on the predictions, and fitting the models in periurban communities was difficult because of the sparsity of high-resolution GSV images. Using GSV imagery for estimating dog populations is a promising tool, especially in urban areas. Citizen scientists can help to generate information for disease control programs in places with insufficient resources.

Free-roaming domestic dogs (FRDs) are among the most abundant carnivores on earth and have coexisted with humans for over 15,000 years, yet increases in negative interactions and the transmission of zoonotic diseases, precipitates calls for population management. Despite significant investment in FRD sterilisation in India, where rabies is endemic, there is limited evidence of its impact on reducing FRD population sizes. Therefore, robust evaluation of the effectiveness of fertility control programmes is necessary. To address this, we implemented a Before After Control Intervention (BACI) framework in the first multi-site randomised controlled trial for the sterilisation of FRDs. We conducted single intensive sterilisation campaigns in five areas, achieving female sterilisation coverages of 58–66%. We observed a decrease in puppies and lactating females and a reduction in residents’ reports of barking, a common problem associated with FRDs. There were no significant differences in adult FRD counts between intervention and control sites during the 2-year follow-up. However, unmeasured immigration into and emigration out of study areas may have confounded counts. One-off, albeit intense, sterilisation campaigns in open populations require substantial investment and are unlikely to reduce population size in isolation, though there may be some reduction in problematic behaviours and improved animal welfare.

Domestic dogs can affect human health through bites and pathogen transmission, particularly in resource-poor countries where dogs, including owned ones, predominantly roam freely. Habitat and resource selection analysis methods are commonplace in wildlife studies but have not been used to investigate the environmental resource use of free-roaming domestic dogs (FRDD). The present study implements GPS devices to investigate habitat selection by FRDD from an urban site and a rural site in Indonesia, and one urban and two rural sites in Guatemala (N = 321 dogs). Spatial mixed effects logistic regression models, accounting for heterogeneous distribution of the resources, showed that patterns of habitat selection by FRDD were similar across study sites. The most preferred resources were anthropogenic, being buildings and roads, which implies selection for human proximity. Vegetation and open fields were less preferred and steep terrain was avoided, indicating that FRDD were synanthropic and that their space patterns likely optimised energy use. Results presented here provide novel data on FRDD habitat selection patterns, while improving our understanding of dog roaming behaviour. These findings provide insights into possible high-risk locations for pathogen transmission for diseases such as rabies, and can assist management authorities in the planning and deployment of efficient disease control campaigns, including oral vaccination.