The Prevalence of Parasites in the Domestic Pigeons (Columba livia domestica) in Zakho City, Kurdistan-Iraq

Pigeons have accompanied humans since ancient time because they are used as a source of food, pets, hobby, and religious symbols. Pigeons have shown high prevalence rate of infection with gastrointestinal helminths and protozoan. This study was conducted to evaluate the prevalence of parasitic infections in the domestic pigeon (Columba livia domestica) from October, 2017 to April, 2018, purchased from bird market of Zakho City, Kurdistan region. The samples were taken from 50 adult pigeons (28 males and 22 females). The birds were transferred to Parasitology Laboratory, Faculty of Science, Zakho University. In the laboratory, each bird was sacrificed and immediately the feather and skin of under wings, chest and the rest of the body was examined for ectoparasites. The collected ectoparasites were preserved in 70% alcohol for further study. The sacrificed birds were dissected and their intestine and contained were examined for the presence of parasites. The results revealed a total rate of 76% of infection with ectoparasites, which included three species of lice, namely: Columbicola columbae (56%), Companulotes compar (36%) and Hohorstiella lata (10%). Regarding helminths, cestodes were the only helminths found in this study with a rate of 16% (8/50). Three species of cestodes were recorded, they included: Raillietina cesticillus(14%), Raillietina echinobothrida(4%) and Choanotaenia infundibulum (2%). Further studies are required to evaluate the effect of the recovered parasites on this host and their transmission to other poultry flocks and human.


Introduction:
Pigeons belong to order Columbiformes, which are domesticated birds that can be found in almost every town and city around the globe except for the poles (1,2). This bird has accompanied humans since ancient time, and has close communication with humans, since is used as a source of food, pets, hobby, and religious symbols and recently as a laboratory animal (3,4). It feeds on food items, which include grains, earthworm, and insects (5). Like other domestic poultry, pigeons have shown high prevalence rate of infection with gastrointestinal helminths and protozoan (6). Pigeons are able to fly for far distances, they can carry many parasites such as fleas, ticks, mites, and other parasites (7,8,9). These parasites can survive under several environmental conditions and live in the body, the skin and between the feathers of the birds (10). Pigeons have a major role in spreading of infection and transmission of zoonotic diseases for people such as Newcastle disease, cryptococcosis, coccidiosis, toxoplasmosis and salmonellosis as well as being a reservoir of many parasitic diseases for poultry and other economic birds such as, chickens and ducks (11,12,13). Also, the ectoparasites and endoparasites that cause morbidity and mortality in these birds produce some symptoms such as weakness, loss of weight, anemia diarrhea and even the death of the birds (14,15). Endoparasites are the most important diseases occurring in poultry especially cestodes (16). Only one study has been performed in Duhok City on the prevalence of pigeon parasites (17). The aim of this

Materials and Methods:
The study was conducted between October 2017 and April 2018 in Zakho City, Duhok Province, Kurdistan Region/ Iraq. Fifty adult domesticated pigeons from both sex (28 males and 22 females) were purchased from bird market to which birds from different parts of Zakho City are sold. The birds were transferred to the Parasitology laboratory in the Faculty of Science, Zakho University. In the laboratory after sacrificing the birds, each bird was kept in a polythene bag, the ectoparasites were collected after sacrificing the pigeon, in addition, the feather of the head, neck, under the wings, legs and cloaca of each bird was inspected to look for more ectoparasites. The obtained parasites were preserved in 70% ethanol then; later on, they were identified according to the identification keys (18. 19).

Postmortem Examination for Endoparasites
This was done after decapitation, the abdominal and thoracic cavity of each pigeon was opened, and this was followed by systemic autopsy examination which includes the esophagus to the gizzard, the small intestine (duodenum, jejunum and ileum), the caeca, and the ileo-caeco-colic junction to the cloaca. Each section was kept in a clean Petridish, then opened longitudinally and the contents were washed with phosphate buffer (pH 7.2-7.4), then passed through 100 μM stainless steel sieve. The mucosa was scraped to collect the helminths embedded in the mucosal layer. Finally, the contents were examined under stereoscopic microscope and all of recovered helminths were counted. The recovered helminths were cestodes only ( Fig. 1), each cestode before being fixed was measured and cut into various pieces, the scolex was placed between two cover slips while the proglottids were placed between two slides, tight with a thread, then fixed in 70% ethanol in fully labeled containers for further processing and identification.

Staining and Identification of Cestodes
The fixed cestodescolices and proglottids were placed in descending alcohol series (50 and 30) then washed several times with tap water and then were stained with aceto-carmine stain. Following staining, they were passed through a series of ascending ethanol (30, 50, 70, 90 and 100 %) and cleared in xylol for 15-30 minutes depending upon the consistency of the material mounted in Canada balsam or DPX examined under light microscope at 10X magnification then identified according to dependent key (19).

Results and Discussion:
In this study only ectoparasites and cestodes were isolated from infected pigeons, other parasites were not found.
Ectoparasites: The total rate of infestation with ectoparasites was 76 % (38/50 of pigeons examined) some were infected with more than one species of parasites as shown in Table 1. The recorded ectoparasites were three species of lice which have been collected from different parts of the body (head, neck, under the wings, legs and cloaca), they included: Columbicola columbae, Companulotes compar and Hohorstiella lata (Fig.  2). The prevalence rate of infestation with ectoparasites reported in this study is much higher than the rate (6%) recorded by (17) in Duhok city. Slightly lower rates of infestation with different species of lice have been reported in Turkey [20], in Nigeria (21), in Tanzania (22) and in Bangladesh (23) which were 52, 60, 62 and 67%, respectively. While in Libya a higher rate (89%) of infestation with ectoparasites was reported (24).
The highest rate (56%) in this study was with Columbicola columbae, whereas, the two other lice species (Companulotes compar and Hohorstiella lata) were found at lower rates, 36% and 10%, 212 respectively. The rate of infestation with each species of lice recorded in the present study is higher than those recorded in Duhok which was 6% infestation with Columbicola columbae (17) and also in Bangladesh which was 21% (23). Studies performed in Spain (25), in Libya (24), in Iran (26,10), in Colombia (27), in Bangladesh (28) and in Ukraine (29) recorded rates of 100%, 82%, 79.41%, 78,40%, 64%, 50% and 100%, respectively. Also Ukraine (29) recorded higher infestation rate of Hohorstiella lata and Companulotes compar (72.7 and 41.8%, respectively) than the rates of the present study. Lice cause damage by chewing feathers as they squeeze between the barbs of the feathers and they are more commonly seen in outdoor housed birds (30).
Regarding gender, the rate of infestation in males was higher than females (55.26% versus 44.74%). While in Nigeria (21) reported equal rates in both sexes. In a study in Turkey (20) a higher rate of infestation was reported in females than males (54.5% versus 48.9%). The higher rate in males is attributed to more susceptibility to infection than females and they are more affected by infestation and this could be due to behavioral differences, with one gender coming into contact with sources of infection more than the other. Furthermore, it has also been ascribed to the association between testosterone and the immune system, although the exact mechanism of action is unclear, but evidence suggests that testosterone has an immunosuppressive role which would hamper the elimination of the parasites (31).

Cestodes
The rate of infection with different species of cestodes is shown in Table 3, in which 8 out of 50 (16%) pigeons examined, were found infected by three species of cestodes. These cestodes inhabited the small intestine, which included: Raillietina cesticillus (Fig.3), R. echinobothrida (Fig.4) and Choanotaenia infundibulum (Fig.5). Higher rates of infection with cestodes in pigeons have been reported in Kurdistan and other parts of Iraq, such as, (17) in Duhok and (32) in Baghdad which were 22% and 17.14%, respectively. Much higher rates of cestodes infection have been reported in Diyala (33), in Babylon (34) and in AL-Dewaniya (35) which reported rates of 73.01%, 57.97% and 46.31%, respectively. Also, in Egypt, a rate of 30.9% was reported (36).
In this study, the highest (14%)rate of infection was with R. cesticillus, while both R. echinobothrida and Choanotaenia infundibulum were recorded at low rates (4% and 2%). Similarly (21) in Nigeria recorded high infection rate (26.7%) with R. cesticillus. Whereas, in a study in Duhok and another one in Nigeria high rates of R. tetragona were recorded (22% and 27.1%) (17,7) respectively. In Baghdad (32) and in Egypt (36), high rates were reported (17.14% and 17.7%) with R. echinobothrida. Most pigeons were infected with cestodes and 75% of cestodes were Raillietina spp. (37,38). Cestodes cause severe histological changes in the host, they can cause lesions including congestion, inflammation, nodules formation in intestinal mucosa and pin point hemorrhages (39). Different species of cestodes cause severe destruction of villi, desquamation and degeneration of epithelial cells (40,39).
With respect to gender, females showed a higher rate (62.5%) than males (37.5%). This finding is similar to the results obtained by (41) in Erbil, (34) in Babylon, (35) in AL-Diwaniya and (42) in Nigeria; in all these studies higher rates of infection were found in females. On the other hand, the present results disagree with a study performed in Diyala (33) and in Brazil (43) which reported high rate of infection in males.   Table 4 shows the rate of mixed infection of cestodes in the pigeon. Single infection accounts for 12%, while double ones were recorded at low rate (4%). Similarly in Nigeria (7) and Iran (44) higher rates of single infection than double infections were recorded. The prevalence of cestodes in pigeon may be attributed to the abundant presence of the intermediate hosts of these parasites; such as beetles, pill bugs, ants, earthworms and snails which form part of the diet of pigeons, which can easily infect the birds via their diet (5).

Conclusion:
It is concluded from this study that the examined pigeons showed high infestation rate (76%) with ectoparasites, included three species of lice. Regarding endoparasites only cestodes (three species) were recorded at a lower rate(16%). Some pigeons were infected with more than one species of parasites.