To the authors’ knowledge, this is the first of epidemiological report of screwworm myiasis in feral swine from South America. Myiasis cases in feral swine were reported by hunters in the Artigas and Salto provinces of Uruguay between April 2017 and April 2020. Of the 618 swine examined, 27 were infested with maggots. Screwworm infestation prevalence (4.36%) in feral swine was relatively higher than the estimated 2-3% in wildlife reported by Lindquist (1937), and lower than the >5% recorded in domestic pigs in Yucatan, Mexico [29]. The prevalence reported here is similar to that in sheep (5.7%) and cattle (3.4%) in Uruguay [24].
Screwworm cases were detected primarily in large male feral swine, and primarily in wounds that the hunters suspected as being the result of fighting between males. Dominance behavior in swine includes the males lining up facing each other and pushing at the shoulders, which can leave large lacerations due to their tusks and biting the neck, ears, and face (Figure 2B)[30]. These opportunities to lay eggs were exploited by screwworm female flies because 41% of the myiases occurred in those body parts of the host. Wound infestation in males associated with lesions resulting from feral swine infighting was also reported to be common in before screwworm eradication Florida was accomplished [6].
Genital myiases in post-birthing females and in juvenile navels are very common in livestock and a primary concern to ranchers. Of the feral swine harvested in this study, only one female with genital myiasis and one juvenile male with naval myiasis were observed. It is possible that in feral swine these are not common sources of myiases, or that these were not commonly observed because they lead to mortality. Navel myiases may have also been underreported, as more adult animals were harvested.
Hunters who participated in this study reported that, although myiases are common in feral swine, they did not observe myiases causing serious morbidity or mortality (A typical myiasis in feral swine is shown in Figure 2B). Physically, feral swine have thick skin that could inhibit the formation of myiasis and be inhospitable to screwworm larvae. Additionally, male swine develop thick layers of skin and cartilage near the shoulder, called shields [20], which protect males during dominance fights and may also inhibit screwworm development (Figure 2C,D). Feral swine behavior may also prevent or treat myiases. Wallowing has many benefits to the animal including thermal regulation, UV protection, and protecting against ectoparasites and biting flies [31]. Screwworm larvae in a myiasis are surrounded by fluid but they must have exposure to air through their terminal spiracles, thus coating a myiasis in mud or water could suffocate larvae [32]. Coating a wound in mud could also prevent release of odors that attract gravid female screwworm flies to a wound and stimulate oviposition. Feral swine also exhibit a rubbing behavior associated with wallowing that could remove unhatched egg masses or larvae close to the surface. They also soak or swim in water, behaviors that have been observed in deer to help clean myiases [15]. Thus, it is possible feral hogs also intentionally soak to remove screwworm larvae.
Feral swine that survive infestation could play an important role in the dissemination of screwworm. Their home range can be over 400 ha and feral swine movement is not inhibited by rivers [33]. It was reported during this study that during some hunting operations in parts of Artigas Department where the Cuareim river serves as the international boundary, feral swine escaped by jumping and swimming to the bank of the river on the Brazilian side of the border. It is probable that screwworm infestations acquired in Uruguay, Argentina, or Brazil could be carried to a bordering country where the larvae would crawl off and pupate. This presents the potential for a transboundary zoonotic disease issue. The results from this study highlight the ability of feral swine in South America to maintain screwworm populations. If one of these nations were to begin a control or eradication program, feral swine would be a source for re-infestation.
Cooperation with local hunters through ProJAB enabled records of screwworm infestation in feral swine, which stresses how research and extension efforts facilitate collaboration between groups that deal with issues at the livestock-wildlife interface. This public-private partnership also involves education of the hunters on practical aspects of veterinary public health to mitigate risks associated with exposure to zoonoses harbored by feral swine in Uruguay [20]. Hunters were made aware of measures to avoid the dispersal of screwworms and to manage the risk of human and domestic animal exposure to infestation. Hunting feral swine often occurs at night and the hunters transport the harvested animals to their homes and leave them hanging until morning when they are cleaned and processed. During this time the 3rd instar larvae would be able to crawl off and pupate near the homes of the hunters increasing the presence of screwworm adults in the vicinity of the hunters’ homes. In Uruguay, up to 818 human cases of screwworm myiasis can be recorded annually with the majority of cases affecting rural populations [24]. This stresses the One Health relevance of screwworm myiasis, which in the region is considered a neglected zoonosis [34].
All the larvae collected from the myiasis cases in feral swine were identified as C. hominivorax, with no secondary species present. Screwworm cases reportedly contain larvae of species in the families Calliphoridae, Sarcophagidae, and Muscidae that cause secondary myiasis [35]. In myiases with secondary species, the primary screwworm C. hominivorax is found feeding on living tissues while the secondary species are at the wound periphery consuming necrotic tissues. The absence of secondary fly larvae in infested feral swine could be due to the same factors mentioned previously for the low mortality associated with myiases. If myiases are not persistent and tissues do not become necrotic, the development of secondary infestation would be unlikely.
Seasonal changes in temperature and precipitation have been correlated with screwworm prevalence. However, the patterns are dependent on local climates and should not be generalized. Screwworm infestation in this study correlated with higher monthly average temperatures, and fewer cases were detected in winter months with low temperatures. These observations are similar to the seasonal variations in screwworm prevalence in the United States prior to eradication [36]. An increase in infestations associated with higher temperature is concerning because it has been estimated that current global change trends could result in an increase in temperatures in Uruguay of up to 3 degrees Celsius by 2100 [37]. Under this scenario that has been contemplated for other parts of the American continent [38], the risk for screwworm infestation could extend in the year thereby reducing the efficacy of seasonal birthing currently practiced by livestock producers in parts of Uruguay with a more temperate climate to reduce screwworm cases. The apparent seasonality of myiases in feral swine mirrors prevalence patterns in livestock, which suggests that screwworms could persist in the environment by infesting feral swine alone in in Uruguay, which was documented in Florida before population control of feral swine and screwworm eradication took place. Total monthly precipitation was not correlated to myiases prevalence as has been seen in screwworm surveys in tropical countries such as Panama or the Caribbean [39,40]. However, the risk for screwworm outbreaks where domestic pigs and feral swine are present must be noted. One pet pig was infested during the 2016 outbreak in Florida [18], and feral swine also thrive in Panama where the screwworm barrier zone exist to prevent the reinvasion of Central and North America through the continental mainland [41].