Seropositivity and Risk Factors Associated with Toxoplasma gondii Infection in Wild Birds from Spain

Abstract

Toxoplasma gondii is a zoonotic intracellular protozoan parasite of worldwide distribution that infects many species of warm-blooded animals, including birds. To date, there is scant information about the seropositivity of T. gondii and the risk factors associated with T. gondii infection in wild bird populations. In the present study, T. gondii infection was evaluated on sera obtained from 1079 wild birds belonging to 56 species (including Falconiformes (n = 610), Strigiformes (n = 260), Ciconiiformes (n = 156), Gruiformes (n = 21), and other orders (n = 32), from different areas of Spain. Antibodies to T. gondii (modified agglutination test, MAT titer ≥1∶25) were found in 282 (26.1%, IC95%:23.5–28.7) of the 1079 birds. This study constitute the first extensive survey in wild birds species in Spain and reports for the first time T. gondii antibodies in the griffon vulture (Gyps fulvus), short-toed snake-eagle (Circaetus gallicus), Bonelli's eagle (Aquila fasciata), golden eagle (Aquila chrysaetos), bearded vulture (Gypaetus barbatus), osprey (Pandion haliaetus), Montagu's harrier (Circus pygargus), Western marsh-harrier (Circus aeruginosus), peregrine falcon (Falco peregrinus), long-eared owl (Asio otus), common scops owl (Otus scops), Eurasian spoonbill (Platalea leucorodia), white stork (Ciconia ciconia), grey heron (Ardea cinerea), common moorhen (Gallinula chloropus); in the International Union for Conservation of Nature (IUCN) “vulnerable” Spanish imperial eagle (Aquila adalberti), lesser kestrel (Falco naumanni) and great bustard (Otis tarda); and in the IUCN “near threatened” red kite (Milvus milvus). The highest seropositivity by species was observed in the Eurasian eagle owl (Bubo bubo) (68.1%, 98 of 144). The main risk factors associated with T. gondii seropositivity in wild birds were age and diet, with the highest exposure in older animals and in carnivorous wild birds. The results showed that T. gondii infection is widespread and can be at a high level in many wild birds in Spain, most likely related to their feeding behaviour.

Interaction of diet and habitat predicts Toxoplasma gondii infection rates in wild birds at a global scale

“…Omnivores and carnivores are also exposed to T. gondii when consuming tissue cysts within infected vertebrate prey. Our results provide additional support that tissue cyst carnivory does lead to higher transmission rates (Cabezón et al, 2011; Ferreira et al, 2019; Ferroglio, Bosio, Trisciuoglio, & Zanet, 2014; Hollings et al, 2013), and this result is robust at broad geographical and taxonomic scales. The important role of T. gondii transmission through tissue cysts is also evident from the lower prevalence in aquatic carnivores and omnivores in comparison to terrestrial carnivores and omnivores.…”

“…Furthermore, the duration and range of viability for tissue cysts in carrion is unknown; therefore, species that arrive more rapidly at carcasses, such as corvids (Gomo, Mattisson, Hagen, Moa, & Willebrand, 2017), could be more likely to consume viable tissue cysts, especially if they scavenge preferentially those tissues rich in tissue cysts, such as the brain. Although our results suggest that dietary supplementation by scavenging did not increase infection rates, several studies of Old and New World vultures report very high T. gondii prevalence (Arene, 1999; Cabezón et al, 2011), indicating that specialist scavengers living in environments where background levels of T. gondii are high could be exposed to trophic accumulation.…”

“…Although we could not consider prey composition within each guild specifically, our analyses suggest that globally, avian terrestrial omnivores are at a higher risk of T. gondii infection than carnivores. This pattern contrasts with regional studies, wherein carnivores had higher infection rates than omnivores in birds (Cabezón et al, 2011), marsupials (Hollings et al, 2013) and mammals (Ferreira et al, 2019; Ferroglio et al, 2014). Compared with other dietary guilds, avian omnivores might have an increased risk of exposure to T. gondii because they can be highly synanthropic (Johnson, 2001).…”

The Life Cycle of Toxoplasma gondii in the Natural Environment

“…gondii infection can be present at a high level in many wild birds without any clinical impact, exposure to T. gondii is highest in carnivorous species [99]. High T. gondii seroprevalence is also reported in large predator species as Lynx and the European wildcat [100,101] which is of epidemiological significance because infected felids shed oocysts in the wild environment.…”

Toxoplasmosis: A Widespread Zoonosis Diversely Affecting Humans and Animals

“…Exposure to T. gondii is highest in carnivorous species (Cabezón et al 2011). High T. gondii seroprevalence is also reported in large predator species as lynx and the European wildcat (Sobrino et al 2007) which is of epidemiological significance because infected felids shed oocysts in the wild environment.…”