Ectoparasites and Intestinal Helminths of Pigeons in Medina, Saudi Arabia

Pigeons (Columbiformes: Columbidae) are found around the world except at the poles (Marques et al., 2007). The domestic pigeons, Columba livia domestica, live side by side with humans and are reared as a source of food, hobbies, symbols, and for experimentations (Sari et al., 2008; Mansur et al., 2019). The breeding and resting sites of domestic pigeons, such as house windows and building roofs, harbor ectoparasites that may infest humans, resulting in serious health problems (Haag-Wackernagel and Moch, 2004; Haag-Wackernagela and Spiewak, 2004; Haag-Wackernagel and Bircher, 2010; Boxler et al., 2016). Ecto- and endoparasites can cause severe growth retardation, low egg production, and vulnerability to further infections in pigeons (Dranzoa, 1999). Pigeons can also act as a potential carrier of zoonotic parasites (Cooper, 1990, 1997; Begum and Sehrin, 2011; Karatepe et al., 2011). During infestation with ectoparasites, birds start to pick and scratch to counter the irritation caused by these ectoparasites. Ectoparasites cause distress, allergies, and occasionally transmit infectious diseases (Marques et al., 2007; Sivajothi and Reddy, 2016). Feral pigeons also host ectoparasites that can attack humans; these include pigeon fleas, Ceratophyllus columbae (Haag-Wackernagel and Spiewak, 2004); ticks, Argas reflexus; as well as bed bugs, Cimex lectularius; and red mite, Dermanyssus gallinae (Haag-Wackernagel and Bircher, 2010; Boxler et al., 2016). Pigeon nests may also present a problem, especially when built on human structures, where they can serve as a source of certain pests that migrate into buildings and thus become pests of humans, causing various health problems (Curtis et al., 2002; Haag-Wackernagel and Bircher, 2010). Furthermore, bacteria and fungi pathogens such as Chlamydophila psittaci (Everett et al., 1999), Salmonella, Campylobacter jejuni, and Cryptococcus neoformans are transmissible to humans by pigeons (Schreiber et al., 2015)

Helminths of domestic pigeons are the most deleterious endoparasites responsible for the occurrence of clinical and subclinical parasitic conditions (Marques et al., 2007; Ghosh et al., 2014; Sivajothi and Reddy, 2016). Substantial work on the parasitic infections of pigeons has been conducted in many countries, such as Kuwait, Iran, Uganda, Tanzania, Turkey, the United States, and South Africa, exploring the community of helminths and blood parasites within some members of family Columbidae (Mohammad and AL-Taqi, 1975; Dranzoa, 1999; Sari et al., 2008; Msoffe et al., 2010; Smith and Fedynich, 2012; Pirali-Kheirabadi et al., 2016; Reeves, 2018, Nebel et al., 2020). The effects of factors affecting parasitism, such as the sex of pigeons and season of the year and transmission of, for example, some blood parasites (such as Haemoproteus columbae) by some ectoparasites of pigeons such as Pseudolynchia canariensis, on the prevalence of parasite infections as well as the histopathological lesions of some intestinal parasites have also been investigated (Mohammad and AL-Taqi, 1975; Dranzoa et al., 1999; Sari et al., 2008; Msoffe et al., 2010; Reeves, 2018).

Pigeons are major agricultural pests that damage and destroy crops. According to Hetmański et al. (2011), pigeon populations are significantly increasing in agricultural areas. Pigeons can take seeds at the sowing time, damaging the new emerging sprouts; they also feed on mature crops resulting in a loss in these crops (Johnston and Janiga, 1995). Pigeons also infest a variety of places such as buildings, factories, and statues, and their nests may damage some of these sites. The fecal droppings of pigeons can damage buildings and monuments (Haag-Wackernagel, 1995).

In Saudi Arabia, control and management strategies for coping with feral pigeons in human housing facilities are either nonexistent (among small-holders or owners) or depend on products such as pigeon spikes, netting (bird wire or mesh), wire coils, scare devices (audio or visual deterrents) or the use of gel products or slippery cages on air conditioners to prevent pigeons from landing or roosting on building surfaces. There are no specific governmental guidelines for controlling the nesting and spreading of breeding sites in windows, buildings, and housing facilities.

For Muslims, Medina is a holy city, and pigeon catching is religiously prohibited, so pigeons are widespread throughout the city. Feral pigeons act as disease carriers and/or reservoir hosts and thus constitute a possible source of infection/infestation for humans. Given the existing religious proscription, little effort has been focused on the pigeon-associated parasites in Medina. Therefore, studies concerning pigeons in such societies are urgently needed, not only to identify the most common associated parasites, as well as with other class of pathogens, but also to determine the possible relationships between these agents and relevant human health problems. This is the first study to explore the diversity and abundance of ectoparasites and intestinal helminths of C. livia (Columbiformes: Columbidae) in Medina.

Feral pigeons were collected between October 2018 and September 2019, from the central region of Medina, Saudi Arabia around the following coordinates: 39°41′22″N, 24°25′43″E, in a circle with about 9-km diameter, 30-km perimeter, and an area of about 70 km². Other pigeon varieties (Pakistani, Farensi, Turki, Kori, and Qatifi) were in private facilities nearby the central region of Medina.

Medina belongs to the Jeddah climatic zone, which is hot and humid, with ineffective precipitation. It is subtropical with a Mediterranean subzone and a mountainous subtype (Zuhairy and Sayigh, 1993; Alrashed and Asif, 2015)

Six pigeon varieties of C. livia (Columbiformes: Columbidae) were investigated in the present study. The most abundant was the feral pigeon, C. l. domestica, known locally as the Harami pigeon (Fig. 1A). Ectoparasites and intestinal helminths were collected from the feral pigeon. Five other rare pigeons (Columba livia variety) were subjected only to ectoparasite collection; these pigeons are known locally as Pakistani, Farensi, Turki, Kori, and Qatifi pigeons (Fig. 1B–F, respectively). As Harami pigeons could be found ubiquitously (Fig. 2A–E), they were either trapped or purchased from the central market of Medina, whereas the other pigeon taxa were examined for ectoparasites only at private pigeon facilities.

Thirty-six adults of different pigeon varieties and 18 squabs of feral pigeons (Fig. 1) were examined for ectoparasites. The plumage of all pigeons and squabs was carefully brushed onto white paper for the collection of ectoparasites. For each bird, the feathers of the wings, tail, and regions around the cloaca and underneath the wings and legs were thoroughly examined with a hand lens for any attached ectoparasites. Ectoparasites were collected and preserved in 70% alcohol. For each pigeon variety, the number of ectoparasites was recorded, and the prevalence of infestation and intensity were calculated (Table I). Ectoparasites were identified according to Hutson (1984), Price et al. (2003), and Mansur et al. (2019).

Fifteen adult feral pigeons and 13 squabs were anesthetized with an ether-soaked cotton pad and then dissected and examined for endoparasites. The alimentary canals were removed, transferred to the saline solution (0.85% NaCl), then carefully opened longitudinally and left in the saline solution for 15–30 min. The liver and lungs were also removed, carefully cut into pieces, and placed in saline for the same period. The alimentary canal, liver, and lungs were carefully examined with the naked eye, then with a hand lens, and finally identified with a compound microscope according to Schmidt and Kuntz (1971) and Schmidt (1986).

The collected intestinal parasites (cestodes and nematodes) were preserved in 70% alcohol. Parasites were then transferred to a 0.5% aceto-carmine stain. After staining, the specimens were dehydrated in an ascending series of ethyl alcohols (50–100%). The specimens were then transferred to cedarwood oil for clearing. Thereafter, the samples were placed on clean slides, and drops of Canada balsam were added. Finally, the specimens were covered with glass slips and left to dry.

Three ectoparasite species were collected from different pigeons (C. livia variety) and feral squabs (Table I). Menopon gallinae was the most abundant ectoparasite (Fig. 3J). It infested all except Kori and Qatifi pigeons. Two hundred twenty-six M. gallinae were collected. The prevalence of M. gallinae was 100%, as it infested all examined Harami, Pakistani, Farensi, and Turki pigeons (Table I). On the other hand, Goniodes dissimilis infested Farensi, Turki, and Kori pigeons. The prevalence of G. dissimilis reached 100% in Farensi pigeons and 50% in both Turki and Kori pigeons. One hundred sixty-four G. dissimilis infested the examined pigeons (Table I). Lastly, 47 Pseudolynchia canariensis infested 88.89% of examined feral squabs (Table I). Pseudolynchia canariensis was the only ectoparasite infested feral pigeon squabs.

Fifteen adult feral pigeons and 13 squabs were examined for helminths. A squab, a male and a female were infected with cestodes of Raillietina spp. with a prevalence of 10.71%. Another squab was infected with nematodes of Ascaridia sp. with a prevalence of 3.57% (Tables II and III). All recovered cestodes and nematodes were collected from the small intestine.

The recovered Raillietina spp. (Fig. 3A–G) were actively moving and had an average length of 7.55 ± 2.32 cm (Table III). Raillietina spp. represented the most abundant helminth species infected feral pigeons and squabs in the present study as 48 Raillietina worms were recovered (Table III).

Four worms of Ascaridia sp. (Fig. 3H, I) were collected from the small intestine of a feral squab. The recovered nematode worms were less active than Raillietina spp. The mean length of Ascaridia sp. worms was 1.75 ± 0.21 cm (Table II).

Both the ectoparasites and intestinal helminths of different pigeons were investigated. Menopon gallinae was the most abundant ectoparasite of the examined pigeons, with a prevalence reaching 100% in Harami, Pakistani, Farensi, and Turki pigeons, and G. dissimilis also infected 100% of the examined Farensi pigeons. The high prevalence could be attributed to the cultural and religious customs of this part of the Saudi Arabia, where pigeons are free-ranging animals that move from 1 nest to another. Similar data were recorded by Dranzoa et al. (1999), Adang et al. (2008), and Abdullah et al. (2018), who reported a high prevalence of Columbicola columbae of up to 94.1%.

Because all pigeon varieties except feral pigeon (Harami pigeons) are rare, they are highly cared for, and localized in limited private facilities. Their ectoparasites were less spread compared to those of Harami pigeons. Notably, no infestations were recorded on Qatifi pigeons, which could be attributed to their behavioral and environmental characteristics.

On the other hand, no M. gallinae infections were recorded in Kori or Qatifi pigeons. For G. dissimilis, no infections were detected in Harami, Pakistani, or Qatifi pigeons. It has been reported that G. dissimilis can show an infection rate of 50% in Turki and Kori pigeons. Pseudolynchia canariensis only infected squabs of Harami pigeons, with approximately 89% prevalence. These findings are in accordance with those of da Cunha Amaral et al. (2013). Alkharigy et al. (2018), recorded several ectoparasites, among which M. gallinae infected only 3% of pigeons; P. canariensis was also recorded and was found to infect 1% of pigeons. It was reported by Ghosh et al. (2014), that P. canariensis infected 43% of the examined pigeons. In the present study, the rate of infection with M. gallinae and P. canariensis was much higher than those recorded by Ghosh et al. (2014), and Alkharigy et al. (2018). This difference in prevalence may be because of geographical and temperature variations.

In another study on the ectoparasites of pigeons conducted in Salah Al-Deen Province, Iraq, Aljoburi et al. (2019), recorded M. gallinae infections in 9.4% of pigeons. Reports of similar ectoparasites of pigeons have been documented from Bangladesh (Begum and Sehrin, 2011) and Iran (Radfar et al., 2011), where relatively higher infection rates of pigeons with M. gallinae (60 and 44.11%, respectively) and P. canariensis (63.33 and 63.72%, respectively) have been reported. Comparison of the infection rates of both M. gallinae and P. canariensis showed that they were lower than those obtained in the present study. Marques et al. (2007) reported a 100% rate of P. canariensis infection in examined pigeons from Brazil, which was higher than the rate of infection of P. canariensis (approximately 89%) recorded in the current study.

Begum and Sehrin (2011) observed an increase in the ectoparasite intensity in summer and attributed it to the occurrence of optimum temperature for parasite development and decreased resistance of pigeons to the parasites at high temperatures, resulting in severe infections. This interpretation is in accord with the present results, as the infection rates of the pigeons ranged from 50 to 100% at 36 ± 2 C.

In the present work, feral pigeons were investigated for intestinal helminths. A total of 15 adult pigeons and 13 squabs were examined, and the total prevalence of infection was 14.28% (10.71% of Raillietina spp. and 3.57% of Ascaridia sp.). Similar studies have previously been performed on the intestinal parasites of pigeons. For example, a study by Ahmed et al. (2013) showed that the prevalence of helminth infections reached 51.7% in pigeons in Gharbia Governorate, Egypt. They found that Raillietina echinobothrida and Raillietina georgiensis infected 17.7 and 5.3%, respectively, of the examined pigeons. The prevalence of infection by Raillietina spp. is similar to the findings of our study.

Parsani et al. (2014) recorded 75 and 69% rates of nematode and cestode infection, respectively, in pigeons in India, involving 2 species of nematodes (including 1 Ascaridia sp.) and 5 species of cestodes (including 3 Raillietina spp.). Musa et al. (2011), Begum and Sehrin (2012), Radfar et al. (2012a), Sivajothi and Reddy (2015), Aljoburi et al. (2019), and Mehmood et al. (2019), reported that Raillietina spp. infected 5–100% of examined pigeons. The prevalence of infection reported in the studies of Musa et al. (2011), Begum and Sehrin (2012), Parsani et al. (2014), and Ghosh et al. (2014), was very high compared with those recorded in the present and other studies (Ahmed et al., 2013), and this difference may be because of the pigeon races and sizes, localities, and topographies of the sampling areas, as well as temperature and geographical differences.

Concerning worms of Ascaridia sp., rates of infection recorded in the present work were lower than those reported by Parsani and Momin (2010) and Begum and Shaikh (1987), who reported nematode infection rates of 88.88 and 86%, respectively. Moreover, infections with Ascaridia spp. have been reported to be present in 5–35% of examined pigeons (Begum and Sehrin, 2012; Radfar et al., 2012a, 2012b; Ahmed et al., 2013; Ghosh et al., 2014; Sivajothi and Reddy, 2015; Aljoburi et al., 2019; Mehmood et al., 2019), which is a higher rate than that obtained in the current study, which could be attributed to either the stage of puberty of the pigeons or the season in which the pigeons were examined. Additionally, these differences in the prevalence of infections may be related to different spatial distributions and races of pigeons.

The identification of more than 1 species of Raillietina and at least 1 species of Ascardia in the present and other studies (Musa et al., 2011; Ahmed et al., 2013; Parsani et al., 2014; Aljoburi et al., 2019) supports the worldwide distribution of these parasites in wild pigeons. In the present and many previous studies (for example Radfar et al., 2012a, 2012b; Begum and Sehrin, 2012; Mehmood et al., 2019), it has generally been noted that the prevalence of Raillietina spp. is higher than that of Ascaridia spp., which may be because of widespread intermediate hosts such as beetles, ants, and other local insects.

It is possible that the transmission of parasites among pigeons occurs through food and water contamination (Musa et al., 2011). It was also proven by Begum and Sehrin (2012) that the sex of pigeons is not important in helminth infections, as there are no significant differences between the overall parasite intensity in male and female hosts.

The importance of pigeon-associated complications means that we must learn more about the ways in which pigeons may affect our environment, our lifestyle, and our health. This issue is clearly not a major topic of concern in our community, and there are very little data on such problems in Saudi Arabia. Therefore, it was concluded that pigeon control and management strategies as well as public education should be adopted to reduce the threat of transmission of pathogens and parasites of pigeon to the livestock or to the human population.

The present study shows that pigeons of Medina are infested/infected with both ectoparasites and intestinal helminths. Ectoparasites infested most pigeons examined in the current work. Harami pigeons were infested with both M. gallinae and P. canariensis. Pakistani pigeons were infested only with M. gallinae. However, Farensi and Turki pigeons were infested by both M. gallinae and G. dissimilis. Kori pigeons were infested only with G. dissimilis. Qatifi pigeons were not infested by any ectoparasites. Concerning intestinal helminths, Harami pigeons were infected by both Raillietina spp. and Ascaridia sp. This study will pave the way for more studies associated with infections/infestations of pigeons, which will help authorities to implement necessary and precautionary control measures against pigeon-associated parasitic diseases and subsequently improve the health conditions of the community.

The authors assert all applicable international, national, and/or institutional guidelines for the care and use of animals were followed.