Knowledge of animal visitation to locations where species aggregate is valuable for evaluating potential pathways of inter- and intraspecific transmission of infectious diseases. There is no research evaluating the potential of wallows created by invasive wild pigs (Sus scrofa) as locations of transmission of infectious diseases. We monitored wild pig wallows by using trail cameras to determine the frequency with which wild pigs and native vertebrate species visited wallows and to characterize these interactions for their potential for disease transmission. We placed cameras from 20 June 2016 to 21 September 2016 at 16 individual wallows within 10 wallowing sites. Wild pigs of both sexes visited wallows frequently (115 total visits) for varying durations and exhibited wallowing and drinking behavior. We also observed 12 native mammalian and avian wildlife species using wallows at various frequencies (165 total visits). Of particular interest, nine of these species were observed drinking from wallows. Given the high frequency of wild pig visits to wallows and the drinking behavior they and native wildlife species exhibited, these locations might have an important role in transmission of diseases.
Aggregation of animals at spatially concentrated resources can facilitate transmission of infectious diseases as a result of contact with infected animals or pathogen-contaminated resources (Sorenson et al. 2014). Previous research has focused on disease transmission and contact rates at artificial aggregation points (e.g., man-made watering holes or troughs, wildlife baiting sites, and farm pastures) between wildlife and livestock (Payne et al. 2016; Barasona et al. 2017) and among wildlife species (Campbell et al. 2013). Research is needed to evaluate the potential for disease transmission at natural aggregation sites, such as animal wallows (VerCauteren et al. 2007), in particular, transmission due to use by multiple individuals of the same or different species.
In addition to coating the body surface with mud, wallowing behavior can include urination, ejaculation, and defecation into the wallow (Bracke 2011). Although wallowing is common among many ungulates, use by wild pigs (Sus scrofa) is of particular interest for evaluating disease transmission risks. Wild pig populations have increased throughout their invasive range and are reservoirs for numerous diseases, including brucellosis, Escherichia coli O157: H7, leptospirosis, pseudorabies, salmonellosis, and trichinosis (Hampton et al. 2006; Barrios-Garcia and Ballari 2012; Miller et al. 2017), many of which can be transmitted to humans, wildlife, and livestock. However, little is known about the role wallows may play in transmission dynamics. Previous research has evaluated direct contact rates between wild pigs and wildlife at feeding stations (Campbell et al. 2013) and spatiotemporal overlap or contacts with livestock (Wyckoff et al. 2009; Kukielka et al. 2013; Payne et al. 2016), yet no studies have evaluated inter- and intraspecific visitation rates of wildlife to wallows created and used by wild pigs. The aims of our study were to 1) document visitation by wild pigs to wallows and provide basic demographic and behavioral characterization of interactions with wallows, 2) document visitation by other wildlife and characterize their interactions with wallows, and 3) assess whether these interactions pose risks of disease transmission.
We conducted this research at the Savannah River Site (SRS), a 78,000-ha US Department of Energy facility located near Aiken, South Carolina, US. Habitat on the SRS is dominated by upland pine forests (68%) and bottomland hardwood forests and swamps (22%), with the remaining areas consisting of mixed habitat, developed areas, and clear-cuts. Weather at the SRS is characterized by a warm, humid climate (mean monthly high temperatures: 15.4–33.4 C and mean monthly relative humidity: 63–80%; Kierepka et al. 2016), particularly during summer months. The US Forest Service is responsible for management of both habitat and invasive wild pig populations on the SRS and lethally controls wild pig populations through trapping and hunting with dogs.
We conducted this study from 20 June 2016 to 21 September 2016 when use of wallows by wild pigs would likely be highest due to thermoregulatory needs. We located 10 wallowing sites throughout SRS through opportunistic searches. We defined a wallow as an ovoid depression containing standing water that was used for wallowing by wild pigs on the basis of evidence such as shape, smoothness, tracks, or mud on nearby trees. Wallowing sites often consisted of multiple wallows within close proximity (about 20 m). At each individual wallow within a site, we attached a camera (Reconyx PC900 Hyperfire I camera, Reconyx, Holmen, Wisconsin, USA, or Moultrie M-990i camera, Moultrie Feeders, Birmingham, Alabama, USA) to a tree or post 2–3 m from the wallow. The cameras were set to take three pictures per trigger event, with a 1-min delay between events.
We recorded the number of visits by each species to each wallow and whether wallowing or other behaviors occurred. A visit was defined as any interaction with the wallow, including wallowing, walking though, drinking from, or other contact with the wallow. We defined wallowing as an animal lying in the wallow for any discernible length of time. Wild pigs frequently travel in matrilineal groups, so we conservatively considered all pigs photographed within 30 min of each other to represent a single visit. When possible, we identified individual pigs by morphologic characteristics (e.g., coat color, scars, and size) and recorded sex and age (juvenile, subadult, or adult; Keiter et al. 2017). Because juvenile wild pigs (piglets) do not travel independently of adults and are difficult to sex from photos, we excluded them from comparison of visitation rates between sexes. To allow comparison between species, we standardized visitation data to visits per 100 camera nights. We calculated mean numbers of species interacting with each wallowing site (as defined previously). Because of our interest in the potential for disease transmission, we also calculated both the mean amount of time elapsed between a wild pig wallowing and the next visit to that wallow by another wild pig, as well as to the next visit to that wallow by any other species.
We evaluated whether there was a relationship between the number of individual wallows at a wallowing site and the total number of individual wild pigs (excluding piglets) that visited that location. We considered individual wallows to be part of the same site if they were within 20 m. We created a basic linear regression model in R (R Development Core Team 2014) in which the response variable was the natural log-transformed total number of individual pigs that visited a wallowing site (n=10) and the predictor variable was the number of wallows at the site.
We monitored 10 wallowing sites, consisting of 16 wallows (range=1–3 wallows per site). The mean distance between wallowing sites was 16.8 km (SD=10.3 km, range=1.4–39.2 km). We observed wallows for mean=81.3 d (range=27–98 d), resulting in 1,545 camera nights and recorded 115 visits by wild pigs (7.44 visits per 100 trap nights; Table 1). The median duration of a visit was 1 min (range=1–62), with 91 recorded wallowing incidents. We recorded a minimum of 28 individual adult male and 25 individual adult female wild pigs using wallows; the pigs were accompanied by approximately 28 unsexed piglets. We observed a single wild pig at two wallowing sites, but all other pigs were observed at only one location. On 11 occasions, we were unable to sex an animal from photos. Group size ranged from one to six wallowing individuals (median=1), and when multiple pigs visited, they would often occupy the same wallow simultaneously (Fig. 1). The mean amount of time between a pig wallowing and another visit by wild pigs to that wallow was 171 h (SD=10 h 8 min). Duration of visits by males (median=1 min, range=1–26 min) and females (median=1 min, range=1–62 min) was similar. We observed from 1 to 19 individual adult or subadult pigs using a wallowing site (mean=5.5, SD=5.2); however, the number of individual wallows present did not explain a significant amount of variance in the total number of wild pigs that visited that site (adjusted R2=0.13, P=0.168, df=8).
We also recorded 165 visits to wallows by 12 other species (Table 1). Among mammals, raccoons (Procyon lotor), nine-banded armadillos (Dasypus novemcinctus), coyotes (Canis latrans), and white-tailed deer (Odocoileus virginianus) were most commonly observed (Table 1). Several avian species were also observed at wallows, with American Crows (Corvus brachyrhynchos) and Wild Turkey (Meleagris gallopavo) visiting most frequently (Table 1). The mean time between a wild pig wallowing and another species interacting with that wallow was 74 h (SD=6 h 26 min, range=1–1,222 h, median=20 h 46 min). We observed 10 species drinking from wallows (Fig. 2 and Table 1). In addition, we observed nine-banded armadillos exhibiting wallowing behavior and photographed a Cooper's Hawk (Accipiter cooperi) and a Black Vulture (Coragyps atratus) bathing in wallows. We recorded from two to 10 species (including wild pigs) at each wallowing site (mean=5 species, SD=2.2).
In this study, we found wild pigs frequently used wallows, along with 12 other wildlife species. Many wildlife pathogens (e.g., protozoans, pathogenic bacteria) carried by wild pigs can be deposited into the environment through urination or defecation (Atwill et al. 1997; Hampton et al. 2006; Kaller et al. 2007), which previous research has documented in wallows (Bracke 2011). Infected wild pigs could deposit pathogens in wallows as a result of this frequent and extended contact. In particular, the relatively small size of wallows, as compared with watersheds or drinking water catchments, and relatively frequent use by wild pigs in summer could result in high concentrations of pathogens in wallows.
Wild pigs within the same group often used wallows simultaneously or immediately after each other. Thus, there is high potential for intraspecific transmission of pathogens among wild pigs at wallows, particularly between group members. We also observed numerous pigs drinking from wallows, highlighting the potential for disease transmission, as many pathogens carried by wild pigs can be transmitted through ingestion of contaminated water (e.g., leptospirosis, Salmonella spp., Giardia duodenalis, and E. coli; Hampton et al. 2006). We found male and female wild pigs visited wallows with similar frequencies; thus, both sexes are likely similarly exposed to any pathogens within wallows. We found no relationship between the number of wallows at a wallowing site and the number of wild pigs observed at that location.
Wild pig wallows were visited with varying frequency by 12 native wildlife species, and most species consumed water from active wallows. Although we did not observe drinking behavior by any species with great frequency (Table 1), our cameras were not programed to reliably characterize this behavior. We found the mean time between a wild pig wallowing and another species visiting that wallow was 74 h. The persistence time of pathogens carried by wild pigs is likely to vary based upon their natural histories and environmental conditions, but some pathogens are able to persist for long periods within water (e.g., 12 wk for Cryptosporidium oocysts; Olson et al. 1999). Use of wallows by native wildlife following wild pig wallowing, therefore, could fall within the persistence times of certain pathogens.
On the basis of our results, we suggest that wallows may present opportunities for both inter- and intraspecific transmission of diseases due to frequent and varied interactions with wallows by numerous species and their potential as aggregation sites. However, there remains a need to better understand the role wallows may have in transmission of infectious diseases. We recommend research be conducted to evaluate pathogen levels and persistence within the water and mud of wallows and to relate these levels to infection rates in wild pigs and native wildlife. Such data would provide insight into the risk of disease transmission, as well as determine whether wallows could be used as focal sampling sites for disease surveillance purposes.
We thank the US Forest Service and Savannah River Ecology Laboratory employees, in particular L. Lee, who helped us locate wild pig wallows. We thank the reviewers for constructive comments that improved this manuscript. Funding for this research was provided by the US Department of Energy under award DE-EM0004391 to the University of Georgia Research Foundation.
2Current address: US Department of Agriculture, Animal Plant Health Inspection Service, Wildlife Services, 400 Northeast Dr., Suite L, Columbia, South Carolina 29203, USA
3Current address: University of Nebraska, School of Natural Resources, 243 Hardin Hall, 3310 Holdrege St., Lincoln, Nebraska 68583, USA
4These authors contributed equally to this work and both are considered first authors.