First record of Procyrnea sp. (Nematoda: Habronematidae) in Buteogallus schistaceus (Sundevall) (Accipitriformes: Accipitridae) in Brazilian Amazon

*Corresponding author: Elane Guerreiro Giese. E-mail: lheaufra@gmail.com Abstract Buteogallus schistaceus (Sundevall) is an endemic bird of prey from the Amazon region, with a declining population according to international conservation agencies. The objective of this study was to report the occurrence of a parasitic nematodes in an individual treated at the Ambulatório de Animais Silvestres of Universidade Federal Rural da Amazônia, Belém campus. The animal was captured on campus and showed no resistance to capture. Fluid therapy and deworming were made, later the bird regurgited ten nematodes identified as belonging to the genus Procyrnea Chabaud (1958). Reviewing the scientific literature, it was found that so far there are no records on the helminth fauna of this bird species, which is therefore the first report


Introduction
The Brazilian avifauna comprises over 1900 species among which 91 are birds of prey (Piacentini et al., 2015). This group is essential for population regulation because they are the end of the food chain (Andery et al., 2013). The Slate-colored Hawk Buteogallus schistaceus (Sundevall) is a non-migrant, diurnal neotropical bird of prey endemic to the Amazon rainforest, which occurs from southern Bolivia, through Peru, Ecuador, Colombia, Venezuela, French Guiana and Brazil; in the latter mainly in the states of Amazonas, Pará and Amapá. It is currently declining in its population, despite being classified in conservation status as "least concern" according to BirdLife International (2016). It has a varied diet that includes lizards, snakes and some insects (e.g., orthopteran and moths) (Robinson, 1994).
Procyrnea Chabaud, 1958 contains 60 species described around the world. Of these, 15 have been reported in the Neotropical Region, ten in Brazil ( Table 1). They are parasites of the upper digestive system of birds, especially of the ventricle and proventriculus (Arrona-Rivera et al., 2016). They can cause severe inflammation of the parasitized organ mucosa and consequent organic weakness followed by death (Niemuth et al., 2013).  Cram (1927) Procyrnea waltoni (Freitas & Lent, 1947) Rhea One hundred and seventy years after its original description, there are still no references to the helminth fauna of B. schistaceus in the specialized literature. This fact is of great importance when considering that parasitic action, along with anthropic action, may interfere with its ex situ conservation (Santos et al., 2015). Therefore, the objective of this study was to report the occurrence of Procyrnea sp. in B. schistaceus in the state of Pará, Brazil.

Case report
A young specimen of Buteogallus schistaceus was received for care at the Ambulatório de Animais Silvestres of Universidade Federal Rural da Amazônia, Belém campus. All applicable institutional, national and international guidelines for the care and use of animals were followed. Scientific Collecting Permits were provided by Comitê de Ética no Uso de Animais (CEUA/ UFRA) (Permit Number 23084.022512/2014-18). The animal was observed by a university official on campus grounds (1°27'12.3"S, 48°26'36.5"W), who informed the clinic that the bird appeared to be ill. During capture the animal showed no resistance. At clinical examination, the animal was lethargic, with no escape reflex, with moderate dehydration, weighing 453 g. Direct parasitological examination of the feces did not reveal helminth eggs. The therapeutic protocol consisted of subcutaneous fluid therapy (0.9% saline solution in a total application of 26 mL for three days, combined with a single dose of Vitamin A 20,000 IU) and oral deworming (Praziquantel, Pirantel Pamoate and Oxantel Pamoate in combination) in two applications in a 15-day interval. After the first deworming the animal regurgitated ten nematodes that were collected, fixed in AFA (alcohol-formaldehyde) solution and sent to the Animal Helminthology Laboratory for taxonomic identification. Nematode specimens were clarified with 50% Aman lactophenol and temporarily mounted between slide and coverslip for observation and measurement of morphological characters under light microscope LEICA DM2500 with an imaging capture system. For the taxonomic classification of nematodes, the works of Vicente et al. (1995) and Bagnato et al. (2018) were consulted. Thirty days after admission the animal was returned to the wild.
The nematodes (one male, eight female and one broken specimen) had a thin body, with attenuated extremities and transversely striated cuticle. Mouth with two lips, one ventral and one dorsal, and two lateral pseudolabia with teeth at their anterior border. Esophagus divided into short anterior muscle part and long posterior glandular part. Deirids anterior to the nerve ring. Excretory pore posterior to the nerve ring. Body with two asymetrical lateral alae. Male with unequal and dissimilar spicules. Gubernaculum present. Caudal alae present with longitudinal cuticular thickening. Females with median vulva, of lateral-ventral opening, and pointed tip. These characteristics are compatible with those described for the genus Procyrnea Chabaud, 1958 ( Figure 1 and Table 2). Diagnosis at the specific level was not possible due to the collection of a single male with an extremely curled tail, making it impossible to observe the quantity and disposition of the caudal papillae.
Species of the genus parasitize the upper digestive system of birds, especially the ventricle and proventriculus (Arrona-Rivera et al., 2016). Clinical examination of the bird showed dehydration and low weight, which may be related to Procyrnea parasitism, considering its physiological recovery after the establishment of the fluid therapy and deworming protocol. Failure to observe eggs in the parasitological examination of feces does not rule out this possibility since false negatives may occur in non-specific tests, such as this one.
Based on research in the specialized scientific literature, this is the first report of the occurrence of Procyrnea sp. in B. schistaceus. No other reports of helminth parasitism were found in this bird of prey species, making this the first report of endoparasite in this bird.