1. bookVolumen 59 (2022): Edición 4 (December 2022)
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New Parasitic records of Aves: Phasianidae (Alectoris chukar) in Malakand division northern, Pakistan

Publicado en línea: 30 Dec 2022
Volumen & Edición: Volumen 59 (2022) - Edición 4 (December 2022)
Páginas: 398 - 403
Recibido: 30 Jun 2022
Aceptado: 18 Oct 2022
Detalles de la revista
License
Formato
Revista
eISSN
1336-9083
Primera edición
22 Apr 2006
Calendario de la edición
4 veces al año
Idiomas
Inglés
Introduction

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 ofNo of infectedPrevalenceInfection rate (%)
Infection sites
parasitesbirdsof infected birds
Raillietina echinobothrida734.38.72.1Small intestine
Raillietina tetragona957.1134.2Small intestine
Amoebotaenia cuneate311.402.1Small intestine
Choanotaenia infundibulum111.4 2.1Small intestine
Hypoderaeum conoideum311.402.1Small intestine
Lyperosomum longicauda211.4 2.1Bile duct
Heterakis gallinarum534.38.72.1Intestinal caecum
Ascaridia galli137108.710.6Small intestine
Capillaria phasianina10710138.5Small intestine

Total parasites532941.352.136

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.

Alectoris species

barbaragraecarufachukarReferences
Cestoda
Choanotaenia infundibulumItFrSpBu, IrVasilev, 1992; Al-Barwari & Saeed, 2012; Tarazona et al., 1978; Masala et al., 1986; Belleau & Léonard, 1991
Raillietina tetragonaItTuSpIrAl-Barwari & Saeed, 2012; Masala et al., 1986; Koroglu & Tasan, 1996; Reina et al., 1992

Nematodes
Ascaridia galli It,USTibbits & Babero, 1969; Macchioni & Marconcini, 1982
Capillaria phasianina GrGithkopoulos, 1984
Capillaria contorta SpGrGithkopoulos, 1984; Reina et al., 1992
Ganguleterakis altaica Ka BuVasilev, 1992; Gvozdev, 1956
Ganguleterakis macroura BuVasilev, 1992
Ganguleterakis tenuicaudata FrSpBuVasilev, 1992; Tarazona et al., 1978; Belleau & Léonard, 1991
Heterakis gallinarum Ka, Fr, TuSpIrAl-Barwari & Saeed, 2012; Gvozdev, 1956; Belleau & Léonard, 1991; Reina et al., 1992; Tarazona et al., 1978

Trematodes
Dicrocoelium petroni BuVasilev, 1992
Hypoderaeum conoideum BuVasilev, 1992

Conoidasida
Eimeria kofodi IrAl-Barwari & Saeed, 2012
Eimeria caucasica IrAl-Barwari & Saeed, 2012

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.

HostTotal noInfectedMean weightNon infectedMean weight
Male2312545.3 g11557.6 g
Female4717463.5 g30478.7 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.

Fig. 1

Map of northern Pakistan showing administrative details and site of the study area.
Map of northern Pakistan showing administrative details and site of the study area.

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

Helminthes parasite species reported in chukar and Alectoris species worldwide.

Alectoris species

barbara graeca rufa chukar References
Cestoda
Choanotaenia infundibulum It Fr Sp Bu, Ir Vasilev, 1992; Al-Barwari & Saeed, 2012; Tarazona et al., 1978; Masala et al., 1986; Belleau & Léonard, 1991
Raillietina tetragona It Tu Sp Ir Al-Barwari & Saeed, 2012; Masala et al., 1986; Koroglu & Tasan, 1996; Reina et al., 1992

Nematodes
Ascaridia galli It, US Tibbits & Babero, 1969; Macchioni & Marconcini, 1982
Capillaria phasianina Gr Githkopoulos, 1984
Capillaria contorta Sp Gr Githkopoulos, 1984; Reina et al., 1992
Ganguleterakis altaica Ka Bu Vasilev, 1992; Gvozdev, 1956
Ganguleterakis macroura Bu Vasilev, 1992
Ganguleterakis tenuicaudata Fr Sp Bu Vasilev, 1992; Tarazona et al., 1978; Belleau & Léonard, 1991
Heterakis gallinarum Ka, Fr, Tu Sp Ir Al-Barwari & Saeed, 2012; Gvozdev, 1956; Belleau & Léonard, 1991; Reina et al., 1992; Tarazona et al., 1978

Trematodes
Dicrocoelium petroni Bu Vasilev, 1992
Hypoderaeum conoideum Bu Vasilev, 1992

Conoidasida
Eimeria kofodi Ir Al-Barwari & Saeed, 2012
Eimeria caucasica Ir Al-Barwari & Saeed, 2012

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

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