A Survey of the Ectoparasites Found on Wild Birds in Northwest Turkey

Chewing lice and feather mites are common in all birds and can cause damage to their feathers. This affects their thermoregulation and behavior; reduces the nestling survival, mating success and growth; and influences their coloration. Blood-sucking arthropods, such as ticks or parasitic mites, may cause anemia and secondary or vector-borne infections. Infestations of parasites, such as lice, mites, flies, fleas and other biting insects, cause illnesses and may even cause death, especially of nestlings (Clayton and Walther, 1997; Bush and Clayton, 2018).

Turkey spans 779452 km² that contain 7 major geographical regions and 97 important bird ecosystems encompassing 4% of the country’s total land. Each of the seven geographical regions have different climates, habitats, flora and fauna; and they comprise approximately 460 documented wild bird species, some of which are migrants that summer in Turkey or use it as a flyway route (Anonymus, 2018a). Two of the world’s major bird-migration routes pass through Turkey’s Bosphorus and Canakkale Straits and the valleys of the Eastern Black Sea. Bursa Province (40o 11'N 29^o 04'E), located along the Marmara Sea, lies along the Bosphorus and Canakkale Straits bird migratory flyway and encompasses four important bird areas (Magnin et al., 2000).

The wild birds found in Turkey may be infested with hundreds of different ectoparasite species. The often found ectoparasites on these birds are the louse or feather mite species (Girisgin et al., 2013; Gurler et al., 2013; Dik et al., 2015, 2017) and are recorded from the central or eastern part of Turkey.

Even, number of studies have been carried out on tick infestation of the wild birds (Leblebicioglu et al., 2014; Keskin and Erciyas-Yavuz, 2019), but studies on ked flies infestation is rare, except the study of Erdem et al., (2019).

Therefore, our study aimed to (a) provide information on the distribution of lice/ticks/flies within the study areas, (b) determine the ectoparasite infestation rates in both migratory and resident bird hosts and (c) create coincidence information on ectoparasite species infesting wild birds mainly in northwest of Turkey.

Study area
 
The present study was conducted at the Animal Hospital of Bursa Uludag University in Turkey between January 2015 and February 2019. All of the examined animals were either wounded or sick; but none was snared. All of the birds were separated to avoid contamination.

Most of the birds brought to the hospital were from different areas in Bursa Province, which is a forested area located on the northwestern slope of Mount Uludag. The area has a Mediterranean climate and is generally quite humid (mean humidity: 73%) because of its proximity to the Marmara Sea (Anonymus, 2018b). The wild birds brought to the hospital from outside but near to the area were accepted and included in study population. Balikesir and Bilecik from Marmara Region and Bolu and Zonguldak from Black Sea Region (Fig 1) were the other cities from where the birds were taken.


 
Bird samples
 
The birds used in the study were identified to species using the guidelines described by Heinzel et al., (1995). A total of 188 wild birds belonging to 43 species, 36 genera and 26 families in 17 orders; were included in the study and were examined for ectoparasite infestations.

Birds were examined immediately after arriving. A wide-spectrum insecticide that containing 0.09% tetramethrin and 0.45% piperonyl butoxide was sprayed between the feathers of the wings, tail and head/neck and over a white piece of paper to collect the ectoparasites; these areas were then examined for any remaining ectoparasites (Clayton and Drown, 2001). In addition, the birds were carefully inspected for ticks, especially on the eye, beak and neck regions, which are possible attaching sites (Clayton and Walther, 1997). The detected ticks were manually collected from the birds using a steel tweezers.

The collected ectoparasites were transferred into plastic tubes containing 70% ethyl alcohol and stored in the laboratory until they were examined under a microscope. The data collected from all of the infested birds for each bird species and the ectoparasites were recorded. The lice were dechitinised  in 10% KOH for 24 h, mounted on Canada balsam and identified to species using a light microscope (Nikon Eclipse E600) with the morphological keys of Adam (2004), Adams et al., (2005), Clay (1940, 1958, 1962, 1974, 1977), Clayton et al., (1996), Clay and Hopkins (1954), Pilgrim (1976), Price (1965), Price and Beer (1963), Price et al., (2003), Tendeiro (1973) and Tuff (1970).

After one day immersed in 70% alcohol, the tick and fly species were identified at the species level under a stereomicroscope using the taxonomic keys of Estrada-Pena et al., (2004) for adult ticks, Heylen et al., (2014) and Walker et al., (2005) for immature ticks and Hutson (1984) for ked flies.
 
Data analyses
 
The prevalence of ectoparasites was evaluated for both the bird families and bird species and for each ectoparasite if there was at least one type of collected ectoparasites. The mean abundance and intensity levels were determined for each ectoparasitespecies on the avian hosts.

Ethical approval
 
All applicable international, national and/or institutional guidelines for the care and use of animals were strictly followed. All animal sample collection protocols complied with the current laws of Turkey. Permission to conduct the study protocol and the investigation on the birds was granted by the ethical committee of Bursa Uludag University (No: 2015-06/03) and the Ministry of Forestry and Water Affairs of Turkey on June 29, 2015 (No: 138216).

During the study, 188 birds of 43 species were examined for ectoparasites. Of these, 71 birds (37.7%) of 21 species were migrant and 117 birds (62.2%) of 22 species were resident. A total of 631 lice, four ticks and four flies were collected from 88 birds of 27 species, which corresponds to 46.8% of all birds examined. These birds were infested with at least one ectoparasite with a mean intensity of 8.3, 1.3 and 1.0 per bird for louse, tick and fly species, respectively.

Species-wise, 41 louse species, three tick species and two ked fly species were identified, with the louse species being more prevalent (40.4%) than the fly (2.1%) and tick (2.1%) species. The voucher specimens of lice, ticks and flies were deposited at the Department of Parasitology, Bursa Uludag University, Turkey.

The species of the ectoparasite identified in this study according to parasite orders were presented in Table 1 to 3. Among the lice species, Ciconiphilus quadripustulatus had the highest mean intensity (62.0). Table 1 shows the ecto parasite-free birds together with infested birds.







\Although some of the samples found in the study are similar to those previously made in the area, the new geographic records of lice samples were Fulicoffula gallinula, Ciconiphilus decimfasciatus, Ardeicola ixobrychae and Saemundssonia clayae. The new geographic record for the ked fly sample was Ornithophila metallica. In addition, there are new host records for Turkey: the louse species Pseudomenapon pilosum on common moorhens; the tick species Rhipicephalus sanguineus sensu lato, Haemaphysalis punctata and Ixodes ricinus on white storks, rooks and little owls, respectively and the ked fly species Ornithophilus metallica on Eurasian magpies.

Individually considering the migration status of infested birds, the ectoparasite infestation rate was higher in the residents (52/88; 59.09%) than in the migrants (36/88; 40.90%).

Several researchers throughout the world have studied ectoparasitic infestations in wild birds (Ilieva, 2005; Lyakhova and Kotti, 2011); however, most of these studies from Turkey were on lice (Girisgin et al., 2013; Dik et al., 2017). One of the reasons for this is that lice infestation is common on birds than other ectoparasitic infestation (Bush and Clayton, 2018). In contrast to previous studies, the present study includes all ectoparasites (except feather mites) obtained from both migratory and resident wild birds in Bursa and surroundings, Turkey.

Rehabilitation of wild birds, especially in endangered species requires expertise and special care (Debnath et al., 2018; Aslan et al., 2018). Ectoparasites are great menace to poultry production causing threat to growth, reproduction, behavior, or long-term survival (Clayton and Walther, 1997; Bush and Clayton, 2018). The dynamics of ectoparasite infestations on birds are complicated due to migration or residence, combined with other factors, such as seasonal influences and contact with each other. However, migratory birds may also face additional risks due to perilous journey. In our study, a higher ectoparasite infestation rate was determined on resident birds (59.09%). A previous study in Turkey showed a higher infestation rate on migratory birds (Girisgin et al., 2013). Variation in rate of infestation in different type of birds could be difference in sample size, behaviors, or local conditions of birds (Bush and Clayton, 2018).

Although the ked fly infestation rate was low (2.1%), ked flies (Hippoboscidae) can feed on the host’s blood and cause anemia (Hutson, 1984). Most of the fly species found in this study were similar to those recorded on domestic pigeons in Turkey (Erdem et al., 2019; reviewed in Tezcan, 2020). In addition to the wild pigeons, a less common ked fly species (O. metallica) was detected on a Eurasian magpie, which is the first geographic record in Turkey.

Similar to ked infestation, low tick infestation rate (2.1%) was detected in the present study, which is consistent with that of the other studies conducted in Turkey ranging from 0.5% to 4.36% (Leblebicioglu et al., 2014; Keskin and Erciyas-Yavuz, 2019). Nevertheless, our low numbers of ticks can, all or partially, be from accidental infestation. In addition, most of the detected ticks were larvae and nymphs, similar to those seen in previous studies in Turkey.

The avifauna of an environment plays a critical role in the ecosystem and is involved in the transmission of some zoonotic diseases (Smith et al., 2020); therefore, their ectoparasites may play a role as vectors for spreading diseases. Results revealed numerous species of ectoparasites (lice, ticks and keds) on wild birds in Turkey being heavy infestation on resident birds than migratory. Although these species can be possible vectors, additional research is needed to confirm the related pathogens that they harbor.

Authors thank Prof. Dr. Bilal Dik for his kindly guiding to identify some lice species and advising; and thank Prof.Dr. Levent Aydın for his kindly teaching to identify tick species.

None