Parasitic infections are one of the major health problems of wild birds kept in captivity (RITCHIE et al., 1994; GÓMEZ-PUERTA et al., 2008; OLIVEIRA et al., 2011). Damage to the host and symptoms depend on the pathogenicity and intensity of infection and general condition of the animal (immune competence) (GODOY, 2007). Microorganisms of low pathogenicity can ultimately cause severe clinical disease in birds that are immunosuppressed, stressed, or present concomitant diseases (OLIVEIRA et al., 2011; SANTOS et al., 2011).
Parrots occur from tropical areas to cold regions (GODOY, 2007). Several diseases including endoparasitoses affect these birds (GONZÁLEZ-ACUÑA et al., 2007; SANTOS et al., 2011). In Brazil, helminths of parrots are well known, especially nematodes of the genusAscaridia (GODOY, 2007). Intestinal obstruction due to high parasite loads of Ascaridia sp. is relatively common, causing intussusception and death (GODOY, 2007; GONZÁLEZ-ACUÑA et al., 2007).
Birds of prey are at the top of food chain and are divided in two groups: diurnal (Accipitriformes, Falconiformes) and owls (Strigiformes) (SANMARTÍN et al., 2004; PEREIRA, 2007). Infections caused by endoparasites with no manifestation of clinical signs are common in these birds (PEREIRA, 2007; SANTOS et al., 2011). However, presence of parasites may become apparent in conditions of stress common in captivity, and gastrointestinal infections may be exacerbated by parasites causing diarrhea, anorexia, weight loss, and death (SANTOS et al., 2011).
Parasite identification is important for the knowledge of the most common species infecting wild birds in captivity, in addition to aid in the promotion of quick and efficient implementation of control measures (OLIVEIRA et al., 2011; SANTOS et al., 2011). In this study, we aimed to identify parasites of captive birds (Psittaciformes and Accipitriformes) in the state of Paraíba, Brazil.
The birds analyzed were from the Center for Wildlife Screening (Centro de Triagem de Animais Silvestres - CETAS) of the Brazilian Institute of Environment and Renewable Natural Resources (Instituto Brasileiro de Meio Ambiente e Recursos Naturais Renováveis -IBAMA). The CETAS is an agency responsible for receiving animals handed by the population and/or seized from animal trafficking. These animals are taken to these centers with a recovery purpose and are later sent to zoos that receive particular species or freed in nature. All animals were analyzed on the premises of CETAS located in the municipality of Cabedelo, Paraíba state.
A total of 97 birds necropsied between June and December 2011 were examined for gastrointestinal helminths. The following bird species were evaluated: 54 blue fronted Amazon (Amazona aestiva), 26 orange-winged Amazon (A. amazonica), four red-shouldered macaw (Diopsittaca nobilis), three Caatinga parakeet (Aratinga cactorum), and one scarlet macaw (Ara macao). Psittaciformes came from both trafficking and domestic captivity. Besides the Psittaciformes, nine AccipitriformesRupornis magnirostris (syn. Buteo magnirostris) (Aves, Accipitriformes) from trafficking were also studied.
Some specimens were necropsied immediately after death while others were kept frozen (−10 ° C). During necropsy, helminths were collected solely from the gastrointestinal tract, processed and fixed following the methodology adapted by Hoffmann (1987) and Amato et al. (1991). Parasites were identified according to the following keys: Yamaguti (1963), Petrochenko (1971),Khalil et al. (1994), Vicente et al. (1995) and Anderson et al. (2009).
Of the 97 birds examined, 43 (44.3%) presented nematodes, cestodes and/or acanthocephalans. Prevalence of helminths in Psittaciformes was 45.6% (41/88). Parasites were found in 1/1 (100%) Ara macao, 24/26 (92.3%) A. amazonica, 1/3 (33.3%) A. cactorum, 14/54 (25.9%) A. aestiva, and 1/4 (25%) D. nobilis.
Helminths identified were nematode A. hermaphrodita(Ascaridoidea, Ascarididae) (40/41, 97.6%) (Figure 1) and cestode Raillietina sp. (Cyclophyllidea, Davaineidae) (1/41, 2.4%). A. hermaphrodita was found in the small intestine of all species studied, while Raillietina sp. was found only in the small intestine of A. aestiva. Intensity of infection byA. hermaphrodita was in average 253.5 (ranging from 4 to 503). Intestinal obstruction caused by nematode A. hermaphrodita was the cause of death in 14 of the 40 birds parasitized.
In birds of prey, nematode Synhimantus(Synhimantus) rectus (Spirurida, Acuariidae) (2/9, 22.2%) (Figure 2) was found in the ventricle and proventriculus, while acanthocephalan Centrorhynchus tumidulus (Acanthocephala, Centrorhynchidae) (1/9, 11.1%) was collected in the small intestine. Prevalence of helminths was 33.3% (3/9). Intensity of infection was low: S. rectus with two and four specimens and C. tumidulus with two specimens per animal. In this study, we found prevalence of 45.6%, similar to what was observed (48%) by Freitas et al. (2002) for parrots in captivity from the state of Pernambuco, Brazil.

Figure 2. A) Spicule from male Synhimantus(S) rectus; B) Posterior part from female Synhimantus(S) rectus.
A. hermaphrodita was the most frequent parasite. Hodová et al. (2008) reported that five species ofAscaridia are frequent in Psittaciformes; A. platyceri and A. hermaphrodita are the most common. In Brazil, Pinto et al. (1993) reported A. hermaphrodita as specific of psittacines of genuses Amazona, Anodorhynchus, Ara, Aratinga, Brotogeris, Conurus, Pyrrhura, Psittacus andPionus; this fact corroborates studies on psittacines in Argentina, Chile and Peru (MARTÍNEZ et al., 2003;MASELLO et al., 2006; GONZÁLEZ-ACUÑA et al., 2007; GÓMEZ-PUERTA et al., 2008).
In this study, 14 birds parasitized by A. hermaphrodita died due to parasite infection intensity. Ritchie et al. (1994) reported that ascariasis stands out as one of the most common gastrointestinal parasitic infections in psittacines and is associated with clinical signs such as weight loss, anorexia and, in severe cases, death. González-Acuña et al. (2007) and Hodová et al. (2008) reported intestinal obstruction by A. hermaphrodita as a cause of death in parrots. Hodová et al. (2008) obtained 242 specimens of helminths in necropsied psittacines. González-Acuña et al. (2007) observed severe lesions, with congestion of the intestinal mucosa and increased mucus production.
The prevalence of helminths in birds of prey (22.2%) in this survey was lower than that found in Italy by Santoro et al. (2010), who, through necropsy, reported prevalence of 95% in free-living rapine birds. On the other hand, by fecal examination, Santos et al. (2011) determined prevalence of 13.5% in birds of prey in captivity in Mexico.
In Europe, prevalence of 22.2% was observed for C. tumidulus. Centrorhynchus are considered common helminths in birds of prey, with prevalence ranging from 1.1% in Germany (KRONE, 2000) to 63.6% in Spain (SANMARTÍN et al., 2004) and 100% in Italy (SANTORO et al., 2010).
In the current study, the intensity of infection by S. rectus was low. Santoro et al. (2010) considered intestinal obstruction as a cause of death in the birds studied, which differs from this study. According to these authors,Synhimantus spp. and S. laticeps were associated with erosion and ulcers in the gastric mucosa, whereas infections with more than 100 specimens of Centrorhynchus spp. were associated with enteritis, diarrhea, cachexia, intussusception, and death. On the other hand, Kinsella et al. (1995) reported no injuries related to the presence of Synhimantus sp., S. hamatus, and C. kuntz in birds of prey in the United States, but called attention to the potential pathogenicity of C. kuntz, especially in young birds.
Little is known about the pathogenic effects of parasites in birds of prey (SANTORO et al., 2010). Although clinical signs of parasitism are infrequent, they may become evident under conditions of stress associated with high parasite loads (FREITAS et al., 2002; SANTORO et al., 2010; SANTOS et al., 2011). In this respect, diagnosis and treatment of parasitic diseases should be part of the routine health care of birds in captivity (SANTOS et al., 2011).
All parasites identified in this study were the first record in Psittaciformes and Accipitriformes in captivity in the state of Paraíba. In Brazil,D. nobilis and A. aestiva are presented for the first time as hosts of A. hermaphrodita andRaillietina sp., respectively. Helminth infections in wild birds kept in captivity should be prevented because, in great quantities, they can be lethal to these animals.