Hemosporídeos parasitos (Haemosporida: Apicomplexa) em aves de rapina neotropicais: diversidade, abordagem integrativa e conservação

Abstract

Birds of prey, a group formed by the orders Accipitriformes, Falconiformes, Cathartiformes and Strigiformes, have similar morphological and behavioral patterns, being mainly top predators of the food chain. Birds coming from free living are often parasitized by haemosporidians, hemoprotozoa of the order Haemosporida, however, parasitological studies involving the species of birds of prey of the Neotropics are still scarce. Therefore, the aim of the present study was to know which birds of prey arrived at Wildlife Rehabilitations Centers (CETAS) of Brazil, as well as to investigate the diversity of haemosporidians that infect Neotropical raptors, through an integrative approach that uses morphological, molecular, ecological, phylogenetic, and computational species delimitation analyses, aiming at the conservation of the Brazilian avian fauna. During the years 2004 to 2019, the CETAS of Brazil received 67 species of birds of prey, being 33 of the order Accipitriformes, 17 of Strigiformes, 13 of Falconiformes and four of Cathartiformes. In the MalAvi genetic database were reported 265 sequences of the mitochondrial cyt b gene in 16 of these species of birds of prey, being 218 sequences occurring exclusively in the orders of this group, and 170 unique lineages from a single one of these orders of birds of prey, indicating a possible specificity by the parasitic avian order. In addition to the data obtained by this analysis, blood samples were collected from 155 birds of prey of 23 different species that were received at the CETAS Juiz de Fora. The samples were submitted to hemoparasite research through the evaluation of blood smear and nested-PCR for identification of haemosporidian species. The average prevalence of infection was 58.7% (Strigiformes - 63.75%; Falconiformes - 60.61%; Cathartiformes - 50%; Accipitriformes - 46.15%), being registered for the first time the infection of Strix virgata and Bubo virginianus by Plasmodium nucleophilum; of Pulsatrix koeniswaldiana, Asio clamator and Megascops choliba by Haemoproteus macrovacuolatus; and of Athene cunicularia, Glaucidium brasilianum and Pulsatrix koeniswaldiana by Haemoproteus syrnii. We also obtained 20 sequences of the cyt b gene, eight of them new deposits in the genetic databases. No significant differences or correlations were found between infection prevalence with bird age, season (rainy or dry) and meteorological factors (temperature and precipitation). This study also provides the morphological, morphometric and molecular characterization of Haemorporteus syrnii in owls, and demonstrates that the sequences found of this parasite are grouped in two independent clades well supported, with considerable intra-specific variation and with small morphological and morphometric differences within the population studied, suggesting the existence of potential cryptic species. The histopathological analysis of the owls revealed that the lungs and the skeletal muscle are sites of exo-erythrocytic stages of H. syrnii. The algorithms of computational delimitation of species, a recent tool used in the Haemosporida order, indicated that there is a cryptic diversity of these species occurring in birds of prey, and that despite the need for further studies with these new tools, already demonstrate that there should be a care in the management and reintroduction of infected birds. Studies related to the parasitism of birds of prey by haemosporidians are essential for the development of avian conservation strategies, mainly knowing that a great part of the birds received in the CETAS are reintroduced into the wild. An integrative approach with different methodologies as developed in this study can help in the identification of haemosporidian species, in the understanding of their possible deleterious effects on birds of prey and in the decision making regarding the management of captive birds.