Biodiversity and Prevalence of Parasites of Domestic Pigeons (Columba Livia Domestica) in a Selected Semiarid Zone of South Khorasan, Iran

Trop Anim Health Prod (2012) 44:225–229 DOI 10.1007/s11250-011-0002-3

ORIGINAL RESEARCH

Biodiversity and prevalence of parasites of domestic pigeons (Columba livia domestica) in a selected semiarid zone of South Khorasan, Iran

Mohammad Hossein Radfar & Ehsan Norouzi Asl & Hadi Rezaei Seghinsara & Mohammad Mirzaei Dehaghi & Saeid Fathi

Accepted: 27 October 2011 /Published online: 12 November 2011 # Springer Science+Business Media B.V. 2011

Abstract Five species of nematodes and cestodes were Introduction collected from alimentary canals of pigeons: the nematodes were two species: Ascaridia colombae (16.66%) and Pigeons are seen in more regions of the world except for the Hadjelia truncata (1.96%), while the cestodes were poles. Pigeons live side by side with human and other Cotugnia digonopora (13.79%), Raillietina magninumida animal species in nature, and they are bred as a source of (18.62%) and Raillietina achinobothridia (32.35%); fecal food, as a hobby, symbol, and for experimental aims examination revealed: Eimeria spp. (40.19%) and Crypto- (Harlin, 1994). Pigeons' interaction with man and other sporidium oocysts (2.94%); and blood smears showed: domestic and wild birds makes them a potential carrier of Haemoproteus cloumbae (47/05%); in mouth, throat and zoonotic parasites (Adang et al., 2008). Various parasites larynx: Trichomonans gallinae (57.84%); four species of significantly impede pigeon growth, development and ectoparasites were collected from feathers and subcutaneous productivity that can sometimes lead to the death, specially nodules as follows: feathers: Pseudolynchia canariensis in young squabs (Fatihu et al., 1991). However, little is (63.72%), Columbicola columbae (79.41%), Menopen galli- known about the socioeconomic importance, management nea (44.11%); subcutaneous nodules: Laminosioptes cysti- and health aspects of these birds. Due to perceived little cola (1.96%). From the parasitic fauna identified in this study, importance of pigeons, little attention in terms of research it is imperative to institute an integrated parasitic control has been directed towards the species. In many regions of through constant changing of litter, regular use of antihel- the world, it has been reported that internal and external minthics, anticoccidials and dusting of birds with pesticides. parasites and infections are common in pigeons (Senlik et al., 2005; Marques et al., 2007; Bunbury et al., 2008; Keywords Domestic pigeons . Parasites . South Khorasan . Abreu-Acosta et al., 2009). Information on the parasitic Iran infection of domesticated pigeons in different regions of Iran appears to be relatively little concerned with few published papers and presented mainly as conference M. H. Radfar proceedings or papers only about a single parasitic species Department of Pathobiology, School of Veterinary Medicine, Shahid Bahonar University of Kerman, (Youssefi et al., 2010; Pirali-Kheirabadi et al., 2008). The Kerman, Iran effects of parasitism on birds are often severe including : : retarded growth, low egg production and susceptibility to E. N. Asl (*) H. R. Seghinsara S. Fathi other infections. Other more subtle effects of ectoparasites Shahid Bahonar University of Kerman, Kerman, Iran may also be important. It is only after a thorough study of e-mail: [email protected] these parasites and host:parasite relationships that control measures can be effective. In addition, information from M. M. Dehaghi this study may be a guide to certain control measures, for Department of Pathobiology, School of Veterinary Medicine, Shahid Bahonar University of Kerman, instance, in case of cross-infections whereby control of Kerman, Iran parasites in one host may help in eliminating the same 226 Trop Anim Health Prod (2012) 44:225–229 parasite in another host. Another reason for studying the were immediately placed in a polythene bag and the parasites of domestic pigeons is because they are widespread parasites collected after leaving the pigeons. The ectopar- and might transmit their parasites to wild birds. There are a asites were preserved for identification purposes in 70% number of threatened species of wild birds and exotic alcohol. Subcutaneous nodules of each bird were fixed in pathogens from other birds like pigeons could further 10% potassium, heated for 20 min in a jar containing water contribute to their decline. Therefore, for many reasons, there and their sediments were searched for parasite. is a need to ascertain the parasitic spectrum of pigeons in Iran Routine examinations were made of the entire alimen- and other areas. The aim of this study was to determine the trary tract, respiratory system, liver, heart, kidney and prevalence, intensity, and species of internal and external reproductive truct as follows. The nematodes and cestodes, parasites in domestic pigeon in Birjand area in South removed and washed by water and a number of nematodes, Khorasan of Iran and to obtain information about the effects were cleared in lactophenol for identification and the rest of some factors such as maturity on parasitic infections. stored in 70% alcohol containing 5% glycerin for parasito- logical examination. The cestodes were fixed in 10% formalin and stained with carmine acid for further studies. Material and methods The worms were identified under a light microscope according to helminthological keys by Soulsby (1982). Study area After three washes of the fecal samples, the sediment from each sample was mixed with Sheather's saturated The study was carried out in Birjand, capital South of sugar solution, centrifuged and then examined under a Khorasan province in the east of Iran during October 2008 microscope for the presence of Eimeria oocysts. Detection to September 2009. The samples were taken from 102 of Cryptosporidium oocysts was performed using the pigeons (44 nestlings and 58 adults) from Birjand city. This formalin ether sedimentation method and the modified city (South Khorasan) is geographically located at latitude Ziehl–Neelsen staining technique, and then examined under (32.88°) 32° 52′ 48″ north of the Equator and longitude a microscope for the presence of protozoan oocysts. (59.22°) 59° 13′ 11″ east of the Prime Meridian on the map of the world. The city of Birjand has an estimated population Statistical analysis of 160,000 people. It is a fast growing city, thus becoming one of the major centers in the East of Iran. The city has a dry The computer software, SPSS Version 9.0 for Windows climate with significant difference between day and night (SPSS Inc., Chicago, IL, USA) was used for analysis. To temperatures. The climate of the area is semiarid, with cold compare relative frequency of infection between adult and winters and warm summers and an average annual rainfall of nestling of pigeons, Chi-square tests were used. Differences 167 mm. The mean annual temperature is 16.4°C for Birjand, were considered significant when P<0.05. according to Elias Soltani and Afshin Soltani (2008).

Investigation of the parasites Results

Antemortem examination Parasite species

The blood samples were collected using an insulin syringe The prevalence of parasite species identified in nestlings inserted through a brachial vein catheter. Each sample and adults pigeons is shown in Table 1. Out of a total of provided blood smears, fixed with methanol and stained with 102 pigeons examined, 43 (42.15%) were infected with one Giemsa dyes. The slides were analyzed under light microscopy or more species of helminthes; also, 17 (16.66%) of the using an oil immersion objective. For diagnosis of Tricho- pigeons were infected by nematodes and 26 pigeons monans gallinae, wet and sterile swabs were taken from the (25.49%) were infected with cestodes. Pigeons were surface of the mouth, throat, larynx and crop of pigeons, and infected with one or more helminthes. Pigeons were after preparation slide smears, the samples were studied under infected with one or more ectoparasites (91.17% (93/102)). a light microscope. All parasites were identified according to No trematodes were found in the study. The analysis showed helminthological keys by Soulsby (1982). that worms were significantly (p<0.05) more prevalent in adults than in the nestlings. T. gallinae and Eimeria spp. Postmortem examination were significantly (P<0.05) higher in nestling pigeons than in adults while Haemoproteus columbae and Pseudolynchia The ectoparasites were collected as described by Soulsby canariensis were significantly (P<0.05) higher in adult (1982). Briefly, after killing the pigeons by anesthesia, they pigeons than in nestlings. Also, infection rate of Cryptospo- Trop Anim Health Prod (2012) 44:225–229 227

Table 1 Prevalence of helminthes, ectoparasites and Helminth Adults Nestlings Overall Statistical a protozoa in nestlings and prevalence significance adult pigeons n % n %% P

Ascaridia colombae 14 24.13 3 6.88 16.66 S Hadjelia truncata 2 3.44 0 0 1.96 NS Raillietina magninumida 15 25.86 4 9.09 18.62 S Raillietina achinobothridia 27 46.55 6 13.63 32.35 S Cotugnia digonopora 12 20.68 2 4.54 13.72 S Total helminths 34 58.62 9 20.45 42.15% S Ectoparasites Pseudolynchia canariensis 44 75.86 21 47.27 63.72 S Columbicola columba 43 74.13 38 86.36 79.41 NS Menopen gallinae 26 44.82 19 43.18 44.11 NS Laminosioptes cysticola 2 3.44 0 0 1.96 NS Total ectoparasites 52 89.65 41 93.18 91.17 NS Protozoans Haemoproteus cloumbae 36 62.06 12 27.27 47.05 S NS not significant (P>0.05), S Trichomonans gallinae 18 31.03 41 93.18 57.84 S statistically significant (p<0.05) Cryptosporidium 2 3.44 1 2.27 2.94 NS a Significance of the difference in Eimeria spp. 17 29.31 24 54.54 40.19 S prevalence at the two ages ridium spp. was not significant (P>0.05) in adult pigeons study, Raillietina magninumida was a common cestode of than in nestlings. pigeons, and some birds have heavy infections with these worms. It will be interesting to study the reason for pigeons being more susceptible to R. magninumida as compared to Discussion other birds. Further investigations of health status, blood parameters and growth rate of pigeons will indicate the This is the first study to compare the prevalence and relative effect of these worms in pigeons. The presence of intensity of parasite among pigeon species in the Birjand three species of Raillietina clearly support their cosmopolitan area, South Khorasan of Iran. According to various studies nature in chickens, guinea fowls, turkeys, pigeons, performed in different regions of the world, Ascaridia doves and bush fowls (Soulsby, 1982;Oniyeetal., columbae, Capillaria sp., Dispharnyx sp., Hadjelia truncata, 2001;Auduetal.,2004). Ants of the genera Pheidole and Syngamus sp. and Tetrameres sp. were commonly identified Tetramorium including various beetles, termites, flies and in pigeons (Razmi et al., 2007; Sari et al., 2008; Msoffe et other arthropods in addition to fruits and seeds form the al., 2010). The nematodes encountered (A. columbae and major diets of dove and pigeon (Adang, 1999). The Hadjelia truncata) were of low percentage prevalence. This arthropod portion of the food, by carrying the infective is probably due to the mode of infection as the infective egg stages, serves as intermediate host (Mushi et al. 2000). It dries off when the environment is harsh. Perhaps most of the may, therefore, be right to postulate that the degree of infective stages that got to the final host were through prevalence is determined by levels of the infective stages earthworms as transport host. Despite their low prevalence, present in the intermediate host and, subsequently, their severe hemorragic enteristis, intestinal obstruction, reduction availability to the definitive host. in egg production and, subsequently, death have been known The high prevalence of double infestation of the pigeons to occur (Audu et al., 2004). Hadjelia truncata has been by Columbicola columbae and P. canariensis compared found in the gizzard of a number of bird species in Europe with single infestation may be related to the fact that and Asia. The intermediate hosts are various beetles ectoparasites can cohabit without causing any harmful (Anderson, 2000). This species has also been reported in effects on each other. The interaction of two or more Mashhad area of Iran (Razmi et al., 2007). ectoparasites on the same host may be said to be a low Raillietina spp. are common cestode of pigeons, and interspecific competitive interaction characterized by simul- some birds have heavy infections with these worms that can taneous infestations that may not be detrimental to the two block completely the intestine of infected birds, thus, species. Diversity of bird ectoparasite assemblages may be creating damage on a part of the birds' intestine. In this related to many factors, which may include home range, 228 Trop Anim Health Prod (2012) 44:225–229 behavior, size and roosting habit of the host. The results of the presence of Eimeria labbeana in majority of the samples this study confirmed the findings of other studies performed (Taylor et al., 2007). Four species of Cryptosporidium were in some parts of the world (Mushi et al., 2000). Two birds isolated from the birds: Cryptosporidium baileyi, C. melea- showed the presence of cyst mite (Laminosioptes cysticola) gridis, C. parvum, and C. galli (Sreter and Varga, 2000; Xiao that were reported in pigeons and chicken (Toro et al., et al., 2004). In addition, Cryptosporidium species that are 1999; Eslami et al., 2009). known as water-borne zoonotic protozoans seen in humans The vector of H. columbae is P. canariensis. Both H. and many domestic animals are also encountered in pigeons columbae and P. canariensis are widely distributed in the (Sari et al., 2008). Cryptosporidium infections commonly world, especially in warm and temperate climates (Soulsby, seen in the birds were reported to be found especially in 1982). The results of this study are in line with previous young pigeons rarely at low rates (Ryan et al., 2003; Sreter finding (Gicik and Arslan, 2001; Sol et al., 2000) that older and Varga, 2000). This finding indicates that pigeons could individuals have higher infections of hematozoan parasites be less susceptible to mixed infections in comparison with (that is, H. columbae) than younger ones. There was a chickens. noticeable relationship between the prevalence of H. Pigeons also rapidly attain table weight faster than the columbae and its vector P. canariensis. The closeness in aforementioned meat sources, are easy to breed and keep, their percentage prevalence suggests that most of the make relatively little noise and need little supervision and vectors harbored by the pigeons were probably carrying can are easily kept by novices. This, therefore, suggests its pathogens. A higher prevalence in adults might be the result increasing acceptability and perhaps gives pigeons the of a longer time of exposure to the parasites. However, potential and puts it in an advantageous position to parasite prevalence in nestlings was also high in most of the contribute significantly to this protein demand. Poor animal studied populations, which suggest that infections generally husbandry systems, hazardous seasonal variations such as occurred at an early age. The lower parasite intensity in heat stress, diseases, and malnutrition are only some of the adults, on the other hand, is to be expected if older birds factors preventing availability of increased animal protein acquire a certain degree of immunity against parasites in developing countries. Available reports show that (Merila et al., 1995). pigeons too are often affected by diseases (Natala et al., T. gallinae causes avian trichomoniasis and affects upper 2009). digestive and respiratory tracts (Levine, 1985). Infected Whether these have a more significant effect on the birds frequently show no clinical signs of disease but if health and growth rate of these birds remains to be hosts are young or become immunocompromised and are investigated. From the parasitic fauna seen in this study, it infected with a pathogenic strain, the resulting disease is is imperative to institute an integrated parasitic control usually severe and rapidly causes death (Bunbury et al., through constant changing of litter, regular use of anti- 2008). They can cause granulomatous lesions that occlude helminthics, anticoccidials and dusting of birds with the oesophagic lumen leading to death of birds as a result of pesticides. It is also, important to educate the breeders of severe starvation (Narcisi et al., 1991). T. gallinae was these birds on the need to adhere strictly to these control significantly higher in nestling pigeons than in adults. The measures. reason for the high prevalence may be due to the fact that transmission of the parasite occurs generally when the Acknowledgments This project was funded by the Shahid Bahonar adults feed their young but can occur through food in University of Kerman. We also thank Mr. Mansour Aminzadeh for his technical support. feeders and water. Adult birds may remain infected for a year or more and are a constant source of infection for their young (Soulsby, 1982). References Coccidiosis is one of the important protozoan diseases of birds. The disease has a subclinical course in adults but Abreu-Acosta, N., Foronda-Rodrguez, P., L pez, M. and Valladares, young pigeons exhibit such symptoms of clinical coccidiosis B., 2009. Occurrence of Cryptosporidium hominis in pigeons as fluffy feathers, anorexia, and watery diarrhea with mucus (Columba livia). Acta Parasitologica, 54(1), 1–5. (Levine, 1985). Adang, L.K., 1999. 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