Studies on parasitic prevalence in pet birds from Punjab, Pakistan

Abstract During this one year study, blood and fecal samples of doves (Zenaida asiatica), ducks (Anas platyrhynchos), pigeons (Columba livia), partridges (Alectoris chukar), turkeys (Meleagris gallopavo) and goose (Chen caerulescens) were collected to assess the parasitic prevalence in these birds. The birds were kept at Avian Conservation and Research Center, Department of Wildlife and Ecology, University of Veterinary and Animal Sciences, Lahore. All these avian species were kept in separate cages and their entire body was inspected on regularly basis to record external parasites. For internal parasites, 100 blood and 100 fecal samples for each species were analyzed. During present study, two species of ectoparasites i.e. fowl ticks (Args persicus) and mite (Dermanyssus gallinae) while 17 species of endoparasites; three from blood and 14 from fecal samples were identified. Prevalence of blood parasites was Plasmodium juxtanucleare 29.3%, Aegyptinella pullorum 15% and Leucoctoyzoon simond 13%. Parasitic species recorded from fecal samples included 6 species of nematodes viz. Syngamus trachea with parasitic prevalence of 50%, Capillaria anatis 40%, Capillaria annulata 37.5%, Heterakis gallinarum 28.3%, Ascardia galli 24% and Allodpa suctoria 2%. Similarly, two species of trematodes viz. Prosthogonimus ovatus having parasitic prevalence of 12.1% and Prosthogonimus macrorchis 9.1% were also recorded from fecal samples of the birds. Single cestode species Raillietina echinobothrida having parasitic prevalence of 27% and 3 protozoan species i.e. Eimeria maxima having prevalence 20.1%, Histomonas meleagridis 8% and Giardia lamblia 5.3% were recorded. In our recommendation, proper medication and sanitation of the bird’s houses and cages is recommended to avoid parasites.


Fecal sampling and parasites identification
Fresh fecal samples (n = 100) for each of the captive species were collected and brought to the laboratory for analysis through Smear method.Simple floatation and sedimentation techniques were used to detect parasitic oocytes or eggs.Later on, quantitative fecal sample examination, in term of oocysts per gram of feces was conducted using Macmaster's egg counting technique.The oocytes were repeatedly examined for micrometery.The species were identified through microscopic examination of oocysts and eggs (Atkinson CT et al. 2009).

Blood sampling and parasites analysis
Blood samples (n = 100) from brachial vein of each of the avian species including were collected for endoparasites identification.A drop of fresh blood was placed on a clean glass slide and smear was prepared.Methyl alcohol was used for smear fixation and staining was carried out through Giemsa stain for 5 to 10 minutes.The stained slides were washed with distilled water, dried out and observed under light microscope.Taxonomic keys were used to precisely identify the parasitic species.

Results and Discussion
Temporal and spatial variations in parasitic prevalence are well documented and these variations are attributed with intermediate hosts (Cooper, 2005).Helminth species are highly diverse and are greatly distributed in Asia (Pandey et al. 1992;Bagust, 1994).During present study, a total of nine species of helminthes were recorded including six species of nematodes Syngamus trachea, Capillaria annulata, C. anatis, Ascardia galli, Heterakis gallinarum and Allodopa suctoria, two species of trematodes Prosthogonimus ovatus, P. macrorchis and one species of cestode Raillietina echinobothrida.Ascardia galli, Heterakis gallinarum, and Capillaria annulata (Table 1) are common parasitic species of commercial poultry (Permin et al. 1997).Important helminthic diseases of poultry are ascariodiosis and cestodiosis (Fatihu et al. 1991).One hundred helminth species have been identified from wild and domesticated avian species.Parasitic infections in poultry may result in reduction in growth and egg laying (Van Hemert et al., 2019).Nematodes have been recorded from poultry and other domestic avian species and their presence in birds results in serious infection of digestive tract (Gylstorff and Grimm, 1998).
During present study, Syngamous trachea was recorded from gut content of geese and turkeys and its prevalence was 50%.Glystorff and Grimm (1998) reported Syngamus trachea is responsible for respiratory disorder in chicken, quail, gees peafowl, guinea fowl and turkey.During present study, Ascardia galli was recorded from fecal samples of ducks, dove, turkeys and geese and its prevalence was 24%.Greiner (1997) reported that ascardial roundworm is present in different avian fauna.Most common helminth disease of poultry is Ascariodiosis (Fatihu et al. 1991).Prevalence of Cappillaria annulata was 37.5% while that

Introduction
Commercial farmers prefer confined facilities for birds as density of the birds is higher and these facilities aid to boost their populations.However, higher densities of the birds result in transmission of parasitic agents (Krystianiak et al., 2007) and pathogenic microbes that hinder growth and egg production (Dranzoa et al., 1999).In birds, disease causing species like roundworms reduce breeding success and species like Syngamus trachea, Ascaridia spp, Heterakis isolonche, Capillaria spp.and Eimeria spp.cause coccidiosis (Goldova et al., 1993).Blood parasites viz.Plasmodium spp.and Leukocytozoon spp.are common in feral as well as domestic birds which result in higher mortalities (Aguirre et al., 1986).
In many countries, birds are reared on ground in aviaries where they remain in permanent contact with soil.The soil serves as reservoir for larval insects and helminthes.These factors clearly reflect the presence of wide range of parasites in birds kept in free-range rearing facilities and in turn result in low production (Permin et al., 1997).Amongst parasitic diseases, protozoan diseases especially coccidiosis is top of the list of parasites affecting birds worldwide and result in diarrhea, poor growth, and higher mortalities especially in young birds.Moreover, in confined facilities, birds are more susceptible to parasites and pathogenic microorganisms (Krystianiak et al., 2007).
Poor families keep many avian species as domestic poultry and use these birds as source of food and recreation.However, due to apparent less importance of these birds, little attention in terms of research has been dedicated towards these species and there is paucity of knowledge on health, socio-economic aspects, importance and management strategies of these birds.Understanding parasitic prevalence in poultry birds will aid in developing strategies to manage avian population (Sol and Lefebvre, 2000;Adriano and Cordeiro, 2001).Present study was therefore planned to study the parasitic prevalence in some captive avian species.

Sampling
Present one year study was conducted to check the parasitic prevalence in doves (Zenaida asiatica), ducks (Anas platyrhynchos), pigeons (Columba livia), partridges (Alectoris chukar), turkeys (Meleagris gallopavo) and goose (Chen caerulescens) was conducted at Avian Conservation and Research Center, Department of Wildlife and Ecology, C-Block, Ravi Campus, University of Veterinary and Animal Sciences, Lahore.

Identification of ectoparasites
To determine ectoparasites, the whole body of the birds was fully examined visually on weekly basis and the parasites were collected with the help of forceps and observed and identified under A.KRÜSS Optronic MSL4000-10/30-IL-TL stereo microscope.
Infections with Plasmodium have been identified in all avian orders except Struthioniformes, the Coliiformes and the Trogoniformes (Valkiūnas et al. 2005).The highest diversity of Plasmodium has been recorded form the Columbiformes, Galliformes, and Passeriformes (Valkiūnas et al. 2005;Martinsen et al. 2008).Leucocytozoon has been reported from many avian orders but only some species are pathogenic to their host.Susceptible groups of avian hosts consist of poultry, pigeons, raptors, waterfowl and ostriches (Bennett et al., 1993).Haemoprotozoa are mostly transmitted by blackflies (Atkinson and Riper, 1991).In domestic poultry, only two species of Leucocytozoo i.e.L. sabrazesi and L. caulleryi have been reported (Colley et al. 1971).Leucocytozoon simondi was also recorded during present study.L. simondi is a blood parasite that can cause mortality in domestic geese and ducks and is transmitted by vector black flea (Atkinson and Riper, 1991;Desser and Bennett, 1993).Haemoproteus geneus is equally distributed in birds in all continents except Antarctica because there is no vector for the transmission (Valkiūnas et al., 2005).Dimitrov D et al. (2015) documented that ectoparasites play important role in transmission of diseases and result in great loss to poultry.The fowl tick Argas persicus was also observed during present study.The fowl tick has origination in central Asia (Buczek et al., 2006).Basically, it was an old world parasite but it also exists in new world along with other species viz.Argas miniatus, A. radiates and A. sanchezi.In birds, A. persicus reduces growth and egg yield, also causes weakness and anemia that may lead to death (Khan et al., 2001).Furthermore, in chickens it causes paralysis.One species of chicken mite Dermanyssus gallinae was also observed during present investigation.D. gallinae is continuous blood feeder of chicken, pigeon, turkey and many other avian species.During day time, they live in crevices near host nest, leaving these crevices at night to feed blood of birds.Heavy infection of this mite can decrease egg production in poultry.It also causes anemia, and act as host for secondary infection.of C. anatis was 40%.Capillarian species are thread like nematodea present in the upper area of gastrointestinal tract particularly in esophagous and crop but also found in small intestine (Greiner and Ritchie, 1994;Zucca, 2000) Capillarial species can cause infection in domestic birds where deep litter contains number of eggs in soil or litter (Permin and Hansen, 1998).Heterakis gallinarum is also a nematodal worm and its prevalence was 28.3%.According to Goldova et al. (2006) pheasants and partridges were infected by hetarakis.Menezes et al. (2003) documented that H. gallinarum is responsible for chronic typhilitis and haemosiderosis.H. gallinarum is also capable of transferring protozoan Histomonas meleagridis to birds (Dimitrov D et al. 2015).
Some protozoan parasites have zoonotic potential, and their interaction with infected specimen can cause disease in humans (Slifko et al. 2000).The probability of transmission of zoonotic disease is influenced by so many factors, such as agent stability, population density, animal handling, virulence, route and latent period (Slifko et al. 2000;Marietto-Gonçalves et al. 2008).During present study, three protozoan parasitic species were detected and their prevalence was Eimeria maxima 20.1%, Histomonas meleagridis 8%, Giardia lamblia 5.3% and Eimaria is host specific (Table 2) and mainly found in Galliformes, Columbiformes and poultry (Greiner and Ritchie 1994).Giardia is present in motile trophozoite and cyst stage (Burr et al. 2012).Up to 50% mortality is caused by giardia and it can also lead to poor plumage and can reduce growth (Greiner and Ritchie, 1994).Histomonas is mostly transmitted in embryonated eggs of the cecal nematode Heterakis gallinarum.H. meleagridis is a protozoan parasite which lives in caeca and liver and causes disease in turkeys however it is less fetal in chicken (Dimitrov D et al. 2015).
Three species of parasites viz.Leucoctoyzoon simond, Plasmodium juxtanucleare and Aegyptinella moshkovskii were recorded from blood samples and their prevalence was 13%, 29.3% and 15%, respectively.Haemoparasite are responsible of avian malaria and acute anemia (Vander Heyden, 1996).Avian haemoparasites are pathogenic to their hosts and result in high mortalities, retardation of growth, reproductive failure, reduced productivity and

Conclusions and Recommendation
During present investigation, two species of ectoparasites and 17 species of endoparasites; three from blood and 14 from fecal samples were identified.In our recommendation, proper medication and sanitation of the birds houses and cages is recommended to avoid parasites.

Table 1 .
List of parasites identified in different avian species during study period.

Table 2 .
Parasites, their prediction sites, morphology, life cycle, clinical diagnosis and control measures.