Vet Res Commun (2012) 36:235–238 DOI 10.1007/s11259-012-9530-1

SHORT COMMUNICATION

Identification of parasites in Puffinus puffinus (, ) from Northeastern Brazil

Cristiane Maria Fernandes de Melo & Jaqueline Bianque de Oliveira & Ana Célia Rodrigues Athayde & Antônio Flávio Medeiros Dantas & Thais Ferreira Feitosa & Vinícius Longo Ribeiro Vilela & Danilo José Ayres de Menezes & Paulo Guilherme Carniel Wagner

Accepted: 29 June 2012 /Published online: 26 July 2012 # Springer Science+Business Media B.V. 2012

Abstract Studies on the parasitic fauna of migratory sea Keywords Ectoparasites . Helminths . Wildlife . Sea birds birds of the Puffinus are scarce. Therefore, the aim of this study was to identify parasites of 16 specimens of Puffinus puffinus (Procellariiformes, ) that died during theperiodofJune2011toDecember2011attheWildlife Introduction Screening Center (CETAS) of the Brazilian Institute of Envi- ronment and Natural Resources (IBAMA) in Cabedelo, Para- Brazil shelters a large portion of the biodiversity of marine íba. During necropsy, biting lice and/or gastrointestinal and coastal birds of the world. One hundred and forty-eight helminths were collected in seven (43.7 %) birds. Lice were species are found here, accounting for 28 % of global orders collected in five (31.2 %) birds, and the species identified Procellariiformes, , and , were Halipeurus diversus, Trabeculus aviator, Austromeno- which demonstrates the importance of this country for the pon paululum), Saemundssonia sp. and Naubates sp. The conservation of these birds (Brusque and Vooren 1999). prevalence of helminths was also 31.2 %. The nematodes Besides their maintenance, the local concentration of migra- species were Seuratia shipleyi and Contracaecum sp., and tory is also important within the context of epide- cestodes were Tetrabothrius sp. This is the first record in miologic surveillance. Countries that are on the route of Brazil of Naubates sp., Seuratia shipleyi, Contracaecum sp., these birds are concerned about the entrance of pathogens and Tetrabothrius sp. in Puffinus puffinus. and the consequent occurrence of diseases (Nunes et al. 2006). Contact between these birds and domestic birds can also increase, for both, the risk of infections due to new C. M. F. de Melo : A. C. R. Athayde : A. F. M. Dantas : T. F. Feitosa : V. L. R. Vilela (*) : D. J. A. de Menezes diseases, leading to mortality. Post-Graduate Program in Veterinary Medicine, Among migratory seabirds, the Procellariiformes order Universidade Federal de Campina Grande, stands out, composed of four families: Procellariidae, Patos, PB CEP: 58.108-110, Brazil Hydrobatidae, Diomedeidae, and Pelecanoididae, with a e-mail: [email protected] diet consisting of or marine invertebrates (Brusque J. B. de Oliveira and Vooren 1999). The biology and behavior of Procel- Laboratory of Parasitology, Department of Biology, lariiformes, as well as their parasitic fauna, are unique Universidade Federal Rural de Pernambuco, among birds. The coast of Paraíba state is part of the Recife, PE CEP 52171-900, Brazil migratory route of Puffinus puffinus, P. gravis, and P. P. G. C. Wagner griseus (Procellariiformes, Procellariidae), birds known as Wildlife Screening Center [Centro de Triagem de Animais or silly birds (Brusque and Vooren 1999). Selvagens] (CETAS)/IBAMA Brazilian Institute of Environment Ectoparasites of Puffinus spp. have been well docu- and Natural Resources [Instituto Brasileiro de Meio Ambiente e Recursos Naturais Renováveis], mented, including biting lice as the most frequent and Cabedelo, PB, Brazil abundant (Bourgeois and Threlfall 1979; Zonfrillo 1988; 236 Vet Res Commun (2012) 36:235–238

Foster et al. 1996; Price et al. 2003; Valim et al. 2006). Results Moreover, studies on helminths are scarce (Bourgeois and Threlfall 1979; Foster et al. 1996; Domingues et al. This study indicates, for the first time, the presence of 2005). Naubates sp., Seuratia Shipley, Contracaecum sp., and Tet- Knowledge of the parasite fauna of wild is es- rabothrius sp. in Puffinus puffinus. in Brazil. sential for conservational medicine in the prevention of From a total of 16 birds necropsied, seven (43.7 %) impacts on biodiversity, public health, and environmental were infested by arthropods and/or helminths. In the health. In this regard, the aim of this study was to identify case of migratory seabirds, the physical result of the ectoparasites and helminths of migratory seabirds in captiv- migration process may potentiate the deleterious effects ity at the Wildlife Screening Center (CETAS) of the Brazil- of parasites. In the present study, none of the parasites ian Institute of Environment and Natural Resources identified were related to the cause of death of the birds (IBAMA) of Paraíba. examined. The lice (Arthropoda, Phthiraptera) in both adult and nymph stages were the only ectoparasites found in five Material and methods (31.2 %) of the 16 birds necropsied. Some samples could not be identified at a species level due to the absence of The birds analyzed were maintained on the premises of adult stages or of one sex. In total, the lice collected were CETAS at IBAMA, located in Cabedelo, Paraíba. The birds identified as three species and two genera: Halipeurus diver- were found died and supplied by the local population and sus (Ischnocera, Philopteridae), Trabeculus aviator (Ischno- sunbathers from the beaches or by forest police during the cera, Philopteridae), Austromenopon paululum (Amblycera, period of June to December 2011. Menoponidae), Saedmundssonia sp. (Ischnocera, Philopter- Some were necropsied immediately after death, while idae), and Naubates sp. (Ischnocera, Philopteridae). others were kept frozen (−10 °C) until necropsy. Subse- As to the diversity of lice, multiple infestation or poly- quently, ectoparasites and endoparasites were collected from parasitism was observed in the majority of the birds (80 %). 16 birds of the Puffinus puffinus during necropsies per- Adults and larvae of helminths were collected from the formed at the CETAS and Laboratory of Animal Pathology, proventriculus and small intestine of five (31.2 %) of the 16 Federal University of Campina Grande (UFCG) in Patos, birds necropsied. Nematodes were more prevalent (80 %) PB. Upon physical examination, which precedes the nec- than cestodes. Contrary to what was mentioned regarding ropsies, we observed the presence of lice that were collected ectoparasitism in this study, all birds parasitized were and preserved in ethanol 70°GL for subsequent identifica- infected by only one species of helminth. tion. At the laboratory, the lice were clarified in a battery of The helminths identified were nematodes of the Acuaridae phenol-xylene and then mounted on permanent slides with (Seuratia shipleyi) family, Anisakidae (Contracaecum sp.) synthetic resin (Entellan®). For identification, we used the family, and the cestode Tetrabothriidae (Tetrabothrius sp.) dichotomous keys of Palma et al. (2002), and Price et al. family. (2003). While the necropsies were being conducted, helminths, collected only in the gastrointestinal tract, were gathered, Discussion fixed, and processed following the methodology adapted by Hoffmann (1987), Amato et al. (1991); and Monteiro et al. The prevalence of ectoparasites was lower in this study than (2006). Endoparasites were mounted on slides with perma- that recorded in the state of , United States, by Foster nent synthetic resin (Entellan®) and identified in accordance et al. (1996), who found 100 % of 15 birds parasitized by the with the following dichotomous keys: Yamaguti (1961); P. gravis species. Parasites may directly or indirectly affect Khalil et al. (1994); Vicente et al. (1995); and Anderson et health, also interfering in the reproductive ability and suc- al. (2009). cess of wild birds (Hinojosa-Sáez and González-Acuña Data analysis was restricted to the estimation of prevalence 2005). Biting lice stand out as the most frequent and abun- (Bush et al. 1997). The intensity of infestation and infection dant ectoparasites of the Procellariiformes order, which could not be calculated due to the process of preserving dead are parasitized by about 128 species of the suborders and birds (freezing), as well as the elapsed time between death and Amblycera and Ischnocera (Price et al. 2003), distributed the completion of necropsies, which interfered in the quality into 14 genera of this specific group of birds (Timmermann, and quantity of the parasites collected. This study was ap- 1965; Price et al. 2003; Valim et al. 2006). proved by the System for Authorization and Information on The species of the Halipeurus and Trabeculus genera Biodiversity—SISBIO/Chico Mendes Institute for Biodiver- showed a high degree of specificity with the Procellariidae sity Conservation—ICMBio (No. 29661-1). family of birds, especially those of the Puffinus genus (Foster Vet Res Commun (2012) 36:235–238 237 et al. 1996; Valim et al. 2006). Corroborating this assertion, Stegophorus sp., S. diomedeae, S. stellaepolaris, S. shipleyi, Timmermann (1959)andPriceetal.(2003) indicated that H. Tetrameres sp., larvae of Contracaecum sp., Tetrabothrius diversus and T. aviator lice are specific to P. puffinus. In procerus, T. laccocephalus, T. diomedea, T. filiformis, T. mi- Brazil, these two species are the only ones observed in P. nor, and Tetrabothrius sp. (Bourgeois and Threlfall 1979; puffinus of the collections of the National Museum, Federal Foster et al. 1996). According to Foster et al. (1996), all are University of Rio de Janeiro (Valim et al. 2006). known parasites in P. gravis,exceptS. diomedea, St. stellae- This research was also reported in Puffinus puffinus. polaris, and T. minor. In , Tetrabothrius procerus and T. lice of the genus Austromenopon sp.A.paululumis one laccocephalus were the only species noted in P. creatopus of the most common species of lice in Puffinus birds (Hinojosa-Sáez and González-Acuña 2005). (Foster et al. 1996), and has been identified in 13 Tetrabothrius sp. was also found by Carvalho (2009)on species of birds of this genus, including P. puffinus, P. cetaceans in the northeast. In several cases, parasites are gravis, and P. griseus (Bourgeois and Threlfall 1979; listed among the causes of stranding and death of animals Zonfrillo 1988; Foster et al. 1996; Valim et al. 2006). (Marigo 2003). The association between birds and cetaceans For the genus Naubates, N. harrisoni is noted as occur- was observed by Scherer et al. (2010), who reported the ring frequently in birds of the Puffinus genus, including P. interaction of the species of Stenella frontalis dolphins with puffinus (Foster et al. 1996; Palma et al. 2002). Some lice Procellariiformes seabirds (, , shearwaters, are often lost to other countries. The term astray (from the and the like), where the Puffinus gravis species, considered English, “straggler”) is used to qualify lice that are found the birds that most interact with dolphins in oceanic waters, occasionally in a host that is not its usual host, the result of has been the most frequently seen. natural contamination, without human intervention (Palma Domingues et al. (2005) reported parasitism by Seur- et al. 2002). Furthermore, according to those authors, the atia spp. in P. gravis in Rio Grande, Rio Grande do Sul. term contaminant applies to lice that are transferred acci- According to these authors, the nematodes were fixed on dentally by human action, from a natural host to another the wall of the proventriculus. The Seuratia genus is non-habitual host. In Brazil, the classification was assigned composed of the species S. Shipley, S. marina, S. pro- to the lost species Austromenopon edwardsi and S. bicolor cellariae and S. yamagutii (Mendonça and Rodrigues obtained from skins of P. puffinus and P. gravis, respective- 1968). S. shipleyi, Stegophorus spp. and Tetrabothrius ly, deposited at the Ornithological Collection of the National spp. heteroxenous are parasites, but their biological Museum of the Federal University of Rio de Janeiro (Valim cycles are unknown. et al. 2006). This is the first record in Brazil of Naubates sp. The nematodes of the Anisakidae family are parasites in Puffinus puffinus. of aquatic organisms such as fish, marine mammals and The number of bird species infested by lice ranged from 1 fish-eating birds (Bicudo et al. 2005). The main natural to 3, which was also recorded in P. puffinus and P. gravis definitive hosts for these parasites are piscivorous birds (Bourgeois and Threlfall 1979; Foster et al. 1996). Ectopar- and marine mammals, but the possibility of human in- asitism in birds is determined by physical (temperature and fection, resulting in harmful effects to the body, has humidity), biological (susceptibility), and environmental called attention to the importance of recording the pres- (social and reproductive behavior, and foraging) factors. ence of these parasites in fish sold as food (Barros, et al. Multiple parasitism by arthropods is common both in wild 2006). The C. rudolphii, C. pelagicum, and Contracae- birds and birds in captivity. Captive birds are usually kept in cum sp. species have been identified in birds of the enclosures with large numbers of individuals, favoring the Ciconiiformes, Pelecaniformes, and Trogoniformes orders transmission of ectoparasites (Oliveira et al. 2011). in Brazil (Silva et al. 2005). The prevalence of helminths observed in this study This study indicates the presence, for the first time in (31.2 %) is lower than that reported for P. gravis by Brazil, of Naubates sp., Seuratia Shipley, Contracaecum Bourgeois and Threlfall (1979) (97 %) and Foster et al. sp., and Tetrabothrius sp. in Puffinus puffinus Although (1996) (100 %). Studies on helminth parasites of the parasitism is ubiquitous in wild birds, most of the parasites genus Puffinus are scarce, and studies previously devel- of these animals are unknown, especially in the state of oped were performed with the P. gravis species in Paraíba. The birds studied also showed infestation by Tra- Canada (Bourgeois and Threlfall 1979), United States beculus aviator, Halipeurus diversus, Saedmundssonia sp., (Foster et al. 1996)andBrazil(Dominguesetal.2005), and Austromenopon sp. in addition to the P. creatopus species in Chile (Hinojosa-Sáez Specific studies on the detection and identification of and González-Acuña 2005). Nematodes were more prevalent parasites of migratory seabirds are necessary for under- (80 %) than cestodes, a fact also observed by Bourgeois and standing their interaction with other species of para- Threlfall (1979), and Foster et al. (1996). In prior studies with sites, and their ability to become carriers for other P. gravis in other countries, the helminths recorded were parasites. 238 Vet Res Commun (2012) 36:235–238

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