A review of piroplasmid infections in wild carnivores worldwide: importance for domestic animal health and wildlife conservation

Abstract

Piroplasmids are tick-borne protozoan parasites that infect blood cells (erythrocytes, lymphocytes or other leukocytes) or endothelial cells of numerous wild and domestic vertebrates worldwide. They cause severe disease in livestock, dogs, cats, wild mammals and, occasionally, in humans. Piroplasmid infections are prevalent in wild carnivores worldwide although there is limited information about their clinical and epidemiological importance. There are currently nine recognized species of Babesia, two of Theileria, two of Cytauxzoon and one of Rangelia infecting captive and wild carnivores, including members of Canidae, Felidae, Mustelidae, Procyonidae, Ursidae, Viverridae, Hyaenidae and Herpestidae in the Americas, Eurasia and Africa. However, the number of piroplasmid species is likely higher than currently accepted due to the reported existence of DNA sequences that may correspond to new species and the lack of studies on many host species and biogeographical areas. Indeed, many species have been recognized in the last few years with the advancement of molecular analyses. Disease and mortality have been documented in some wild carnivores, whereas other species appear to act as natural, subclinical reservoirs. Various factors (e.g. unnatural hosts, stress due to captivity, habitat degradation, climate fluctuation or immunosuppression) have been associated with disease susceptibility to piroplasmid infections in some species in captivity. We aimed to review the current knowledge on the epidemiology of piroplasmid infections in wild carnivores and associated tick vectors. Emphasis is given to the role of wild carnivores as reservoirs of clinical piroplasmosis for domestic dogs and cats, and to the importance of piroplasmids as disease agents for endangered carnivores.

Keywords: Babesia; Cytauxzoon; Dog and cat; Piroplasmids; Rangelia; Theileria; Wild carnivores.

Fig. 1

Distribution map of piroplasmid infection in wild carnivores worldwide. (1) High prevalence of Babesia microti-like group in red foxes (Vulpes vulpes) in Europe suggests that this species may be acting as a sylvatic reservoir for these species, or may even be the natural host of the parasite. (2) A canine distemper epidemic among Serengeti lions (Panthera leo) was associated with high levels of Babesia during the 1994 and 2001 outbreaks. (3) Raccoons (Procyon lotor) in USA and Japan may be uncontrolled reservoirs of Babesia sp. and may also participate in the dynamics of human babesiosis caused by B. microti as dispersors of infected ticks. (4) Bobcats (Lynx rufus) and probably (5) cougars (Puma concolor) are the reservoirs of Cytauxzoon felis in North America. (6) The Iberian lynx (Lynx pardinus) is a natural host for Cytauxzoon spp. in the Iberian Peninsula, but due to its reduced population size cannot be considered a relevant reservoir of the parasite. (7) Brazilian wild felids, such as the jaguar (Panthera onca), may also be natural hosts for Cytauxzoon sp. because infection is never related to the presence of clinical signs. (8) Pallas's cats (Otocolobus manul) imported into Oklahoma from Mongolia were found to be infected with intraerythrocytic piroplasms, and DNA sequencing revealed a novel organism, Cytauxzoon manul. (9) A meerkat population in South Africa was found to be frequently infected with Babesia and Cytauxzoon without showing signs of disease. (10) An Asiatic wildcat (Felis silvestris ornata) was found suffering from clinical signs of cytauxzoonosis in Iran