To the authors’ knowledge, this is the first 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 . The prevalence reported here is similar to that in sheep (5.7%) and cattle (3.4%) in Uruguay .
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). 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 fighting was also reported to be common in this wild host before screwworm eradication in Florida was accomplished .
Genital myiases in post-birthing females and in juvenile navels are very common in livestock and a primary concern to ranchers [31,32]. Of the feral swine harvested in this study, only one female with genital myiasis and one juvenile male with navel 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 , 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 . 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 . 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 . 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. Feral swine’s home range can be over 400 ha, and their territorial range is not inhibited by rivers . In fact, 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 areas where both are endemic to act as host for 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 . 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, affecting mainly rural populations . This stresses the need to address the control measures of screwworm myiasis from a One Health perspective, especially since it is a neglected zoonosis in the region .
Ecological classification of myiasis describes screwworm as an obligate primary parasite because it is dependent on a living host and is capable of initiating the myiasis . Secondary, which can be facultative or accidental, myiasis causing species in the families Calliphoridae, Sarcophagidae, and Muscidae are often associated with established screwworm infestations [37,38]. 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. All the larvae collected from the myiasis cases in this study were identified as C. hominivorax, with no secondary myiasis causing species present. The absence of secondary fly larvae in these infested feral swine could be due to the wallowing and swimming behaviors mentioned previously for the low reported mortality associated with myiases. If myiases are not persistent and tissues do not become necrotic, the development of secondary infestation could be less likely.
Seasonal changes in temperature have been correlated with screwworm prevalence in southern Texas in cattle, sheep, and other livestock prior to eradication . 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. 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 . Under this scenario that has been contemplated for other parts of the American continent , 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. 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 [42,43]. However, the risk for screwworm outbreaks where domestic pigs and feral swine are present must be noted. Two pet pigs were infested during the 2016 outbreak in Florida, and feral swine also thrive in Panama where the screwworm barrier zone exists to prevent the reinvasion of Central and North America through the continental mainland [6,44].