Chukar partridge (Alectoris chukar) is a famous game bird belonging to the family Phasianidae. Chukar is a common bird in mountainous areas of the Middle East, Western Europe and Asia (Cramp & Simmons, 1980). They are most prevalent in Asia and have been introduced in areas of North America and New Zealand. Chukar in Pakistan is found in arid, hilly and rocky environments with higher elevation valleys in the inner Himalayan range. In Pakistan it is found in Sindh’s Khirthar range and Punjab’s Chinji Reserved Forest and Margalla Peaks (Ullah & Khan, 2021). The IUCN has classified the chukar Partridge as Least Concern, implying that the species’ population is stable (Bird Life International, 2016). However, population reductions have been reported in some parts of the world; for instance, a small population in Europe is predicted to decline by about 30 % in 11.7 years (three generations) (Bird Life International, 2015). Wild bird populations have declined by an estimated 50 to 60 % on average during the last 40 years (Ullah et al., 2021).
Birds, like other animals, suffer from various diseases. Birds, in the semi-scavenging system are subjected to various forms of parasites, which include various protozoan, helminths, lice, termites, ticks, and fleas. (Rahman et al., 1989). Birds with access to open spaces have a greater variety of parasites (Pandey et al., 1992). Several Alectoris species and subspecies have been the subject of parasitological studies in various regions of the world. Many endoparasite species were obtained and identified from them. Gastro-intestinal protozoans and helminths make up the majority of the first category, with average infection rates broadly clustered around 50 %.
Numerous studies, including those by Ruff and Wilkins (Ruff, 1990) on A. chukar from the United States; Vasilev (Vasilev, 1992) on A. chukar kleini from Bulgaria; and Perrucci et al. (1997) on A. graeca from the United States, Turkey, and Italy, revealed important information. Generally, parasites cause higher mortality due to blood loss, which weakens the host, by diseases caused by toxic endo-parasites, by which arthropods act as mechanical or biological vectors transmitting a variety of pathogens. (Pearson, 1994). Pakistan, like other Asian countries, is still lagging behind. That is to say, most Alectoris species knowledge is narrative and zoogeographical.
The present study, therefore, aims to establish the identity of the helminth parasitic communities of the chukar partridge from northern Pakistan as well as reporting on their prevalence. The sample size employed was much larger than the preliminary ones referred to above, as well as being more representative by obtaining it from several localities and comprising both sexes.
Materials and Methods
A total of 70 chukar partridge A. chukar (23 male and 47 female) were caught by hunters from 18 different localities during the shooting seasons in northern Pakistan from October 2020 to the end of December 2021 (Fig 1). Birds were collected instantly after being shot by hunters, packed in individual plastic bags, and brought to the Department of Parasitology Abdul Wali Khan University Mardan, Pakistan for parasitological analysis. Each bird was given a thorough examination with the results showing that almost all of them were healthy. None of them showed injuries, skin lesions (such as hyperdermatosis, epidermitis and acanthosis) or excessive feather loss or damage. All of the specimens were adult and older than one year, as judged from the observation of the plumage pattern and weight. Sex differentiation was always confirmed by gonadal checking. After decapitation, the abdominal and thoracic cavities were opened, followed by systemic autopsy examination which include, the esophagus through to the gizzard, the small intestine, duodenum, (jejunum and ileum), the caeca, and the ileocecal junction to the cloaca. Each section was opened longitudinally. The intestinal scrapping and floatation methods were used to collect the parasites (Calvete et al., 2003). After being cleaned with 1 % normal saline, the recovered helminths were then preserved in 70 % alcohol. Trematodes and cestodes were all dyed in the lab with acetocarmine and then cleaned with xylene, while nematodes were cleared with lactophenol. Each specimens were morphologically identified using morpho-taxonomic signs and standard identification keys under stereo zoom microscope (SZM405, HT Company Ltd, ILF, UK) (Soulsby, 1982).
Fig. 1
Map of northern Pakistan showing administrative details and site of the study area.
Ethical Approval and/or Informed Consent
All applicable national and institutional guidelines for the care and use of animals were followed.
Results and Discussion
The findings revealed nine helminth species, including four species of Cestode (R. echinobothrida), (R. tetragona) (A. cuneate) and (C. infundibulum), two Trematode (H. conoideum) and (L. longicauda) and three Nematode which include (H. gallinarum), (A. galli) and (C. phasianina). 54.3 % of the specimens examined contained at least one species of helminth parasites. The scientific names of the parasites encountered in both sexes of the host, along with their infection sites and infection rates, are included in Table 1. Only the caecum, small intestine and bile duct were infected internally. No flagellate protozoans, such as Haemoproteus or Plasmodium were found in the upper digestive tracts of any of the chukars studied, and no trematode species were found in the livers or gallbladders of any of the chukar. The mouth, oesophagus and crop of all of the sampled chukars revealed no infection with Capillaria nematodes. In addition, helminth such as the gapeworm Syngamus trachea were not detected in any of the specimens. The host site preference for either of the above species is the small intestine. Their prevalence was moderately higher in male than female hosts.
Prevalence of Helminthes parasite species in chukar partridges.
Endoparasites spp.
No of
No of infected
Prevalence
Infection rate (%)
Infection sites
parasites
birds
of infected birds
♂
♀
Raillietina echinobothrida
7
3
4.3
8.7
2.1
Small intestine
Raillietina tetragona
9
5
7.1
13
4.2
Small intestine
Amoebotaenia cuneate
3
1
1.4
0
2.1
Small intestine
Choanotaenia infundibulum
1
1
1.4
2.1
Small intestine
Hypoderaeum conoideum
3
1
1.4
0
2.1
Small intestine
Lyperosomum longicauda
2
1
1.4
2.1
Bile duct
Heterakis gallinarum
5
3
4.3
8.7
2.1
Intestinal caecum
Ascaridia galli
13
7
10
8.7
10.6
Small intestine
Capillaria phasianina
10
7
10
13
8.5
Small intestine
Total parasites
53
29
41.3
52.1
36
Both davaineid (Raillietina echinobothrid and, Raillietina tetragona) and dilepidida (Amoebotaenia cuneate and Choanotaenia infundibulum) tapeworms were present. The majority of the parasites found were connected to the mucosa by scolices, while some samples were present loosely in the lumen of small intestines. The present study cited R. echinobothrida and Amoebotaenia cuneate and Lyperosomum longicauda for the first time in this host. R. echinobothrida and Lyperosomum longicauda have been found parasitizing house crow (Corvus splendens) in Pakistan (Suleman & Khan, 2016), domestic birds and pigeons in the Nigeria (Edosomwan & Igetei, 2018). Amoebotaenia cuneate was detected in a single specimen in the present study, normally they are responsible for morbidity and mortality in most avian species, but they are of particular importance in poultry (Demis, 2015). R. echinobothrida was first detected in the house sparrow (Passer domesticus) in Iraq with the infection rate of 44.6 %. (Mohammad, 2013). From both domestic and wild birds, a wide variety of Cestodes species have been identified. Chickens (Gallus gallus domesticus), turkeys (Meleagris gallopavo), ducks (Anatidae species), geese (Anser cygnoides), swans (Cygnus), guinea fowl (Numididae), pigeons (Columbidae), pea fowl (Pavo cristatus), ostriches (Struthio camelus), pheasants (Phasianus colchicus), quails (Coturnix coturnix), and other birds are all affected by the diseases they cause (Samour, 2004).
The cestodes R. tetragona is the most common parasites in the present study. Mohammad (1990) found the same results in the black partridge, F. francolinus arabistanicus. This could be because the cestodes’ intermediate hosts, which include a diversity of insects and other invertebrates, are numerous in the animal diet consumed by the hosts. Sawada (1955) mentions 5 species of ants as an intermediate hosts within 26 different invertebrates’ species while Yamaguti (1959) reported 5 species of ants that can be used as intermediate hosts.
Male chukars proved to be more susceptible to parasitization by either of these tapeworms than their female counterparts, although it is unknown if this is because of prevalence or intensity.
One of the two trematode species Hypoderaeum conoideum was encountered in the small intestine while Lyperosomum longicauda was found in the bile duct. When compared to specimens usually seen in Pakistani house crow, the posterior extremities of an adult male of the latter species showed some slight morphological differences (chicken, turkey and duck). The female chukar demonstrated a higher propensity for infection for both of these trematode parasites. Different digenetic trematodes like Dicrocoelium petrovi, Brachylaemus fuscatus and Dicrocoelium sp. are also isolated in adults of other Alectoris species (Vasilev, 1992). The lack of Trichomonas invasion in partridges may be linked to the fact that they do not consume “crop milk” after hatching, without completely ruling out the potential of certain inherent resistance to infection. The helminths of A. chukar in the Malakand division of northern Pakistan suggest that Alectoris spp. are common in their geographical range. All the helminth species have a worldwide distribution and can be found in other Alectoris species (Tables 2).
Helminthes parasite species reported in chukar and Alectoris species worldwide.
It= Italy, Fr= France, Sp= Spain, Bu= Bulgaria, Ir= Iran, Tu= Turkey, US= United States, Ka= Kazakhstan, Gr= Greece
The current study found that the Pakistani chukar population can be parasitized by at least two species of eimeriid coccidians (A. galli and C. phasianina). A similar finding was reported in Poland, C. phasianina was reported for the first time in partridges (Rząd, 2021). Comparatively, the partridge parasites population is more diversified but less dominated by a single parasite species than that of the pheasant parasite community. The literature findings about the higher frequency of Capillaria nematodes in partridges, which are reported below, are supported by our study. The earliest reports of partridge helminths in Poland were found in the 1950s and 1960s. Heterakis gallinarum, Ascaridia compar (Schrank, 1790), A. galli (Schrank, 1788), and four species of Capillaria, including C. caudinflata, have all been found to parasitize the intestines of these birds. Nematodes from the Capillaria genus and the H. gallinarum species are the most prevalent (Kozakiewicz, 1983). The species Heterakis gallinarum (Schrank, 1788) is widely distributed. Pheasant (P. colchicus) is the typical host of this nematode, where it is particularly prevalent in birds i.e., it has been observed in hosts belonging to the Anseriformes and Passeriformes as well as Galliformes. (Fagasi, 1964).
Male hosts had higher rates of parasitism than female hosts, except A. galli. This could be explained by females’ behavioural differences from males, particularly during the egg-laying stage, when females took more insects as food. There are no significant differences in the weights of infected and non-infected male and female hosts. (Table 3).
Weight comparison between infected and uninfected male and female partridge.
Host
Total no
Infected
Mean weight
Non infected
Mean weight
Male
23
12
545.3 g
11
557.6 g
Female
47
17
463.5 g
30
478.7 g
The study reveals that partridges are afflicted with a variety of helminth parasites that may negatively impact their health. Signs and pathology have undoubtedly gained the most interest, but the method of transmission from an affected to a non-infected bird is perhaps the most relevant aspect in terms of possible control methods. To further understand the association between parasites and related diseases in the partridge population, more field research is needed. Strict hygiene measures are also needed to prevent the spread of undesirable pathogens via parasites.
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