New Data on the Chewing Lice (Phthiraptera) of Passerine Birds in East of Iran

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New data on the chewing lice (Phthiraptera) of passerine birds in East of Iran

ARTICLE · JANUARY 2013

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Behnoush Moodi Mansour Aliabadian Ferdowsi University Of Mashhad Ferdowsi University Of Mashhad

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Ali Moshaverinia Omid Mirshamsi Ferdowsi University Of Mashhad Ferdowsi University Of Mashhad

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Available from: Omid Mirshamsi Retrieved on: 05 April 2016 Sci Parasitol 14(2):63-68, June 2013 ISSN 1582-1366 ORIGINAL RESEARCH ARTICLE

New data on the chewing lice (Phthiraptera) of passerine birds in East of Iran

Behnoush Moodi 1, Mansour Aliabadian 1, Ali Moshaverinia 2, Omid Mirshamsi Kakhki 1

1 – Ferdowsi University of Mashhad, Faculty of Sciences, Department of Biology, Iran. 2 – Ferdowsi University of Mashhad, Faculty of Veterinary Medicine, Department of Pathobiology, Iran. Correspondence: Tel. 00985118803786, Fax 00985118763852, E-mail [email protected]

Abstract. Lice (Insecta, Phthiraptera) are permanent ectoparasites of birds and mammals. Despite having a rich avifauna in Iran, limited number of studies have been conducted on lice fauna of wild birds in this region. This study was carried out to identify lice species of passerine birds in East of Iran. A total of 106 passerine birds of 37 species were captured. Their bodies were examined for lice infestation. Fifty two birds (49.05%) of 106 captured birds were infested. Overall 465 lice were collected from infested birds and 11 lice species were identified as follow: Brueelia chayanh on Common Myna (Acridotheres tristis), B. nebulosa on Common Starling (Sturnus vulgaris), B. subtilis on House Sparrow (Passer domesticus) and Tree Sparrow (P. montanus), B. gobiensis on Desert Finch (Carduelis obsoleta), Philopterus pallescens on Great Tit (Parus major), P. montani and Campanulotes compar on Tree Sparrow , P. fringillae on Common Chaffinch (Fringilla coelebs), House Sparrow and Chestnut-shouldered Petronia (Petronia xanthocollis), Sturnidoecus refractariolus on House Sparrow and Common Rock-Sparrow (Pe. petronia), S. ruficeps on House Sparrow and S. rostratus on Corn Bunting ( Emberiza calandra ) and Red-headed Bunting (Emberiza bruniceps). All these lice species were recorded for the first time in Iran.

Keywords: Passerine birds; Lice; Iran. Received 12/02/2013. Accepted 25/02/2013.

Introduction on ectoparasites fauna of birds. The first study on lice infestation of birds in Iran was done by Lice (Insecta, Phthiraptera) are permanent Rafyi et al. in 1968. They identified 15 lice ectoparasites of birds and mammals. Heavy lice species on poultry, pigeons, ducks, geese and infestation has negative effects on health turkeys (Rafyi et al., 1968). After that, 10 new condition and reproductive ability of bird lice species on domestic and wild birds were (Johnson and Clayton, 2003). There are 542 bird reported from Iran (Ardalan, 1971; 1975), while species recorded in Iran, out of which 230 Rak et al. (1975) added 11 new lice species on species are passerine birds (Lepage, 2012). wild birds. In recent years, there have been only Despite having a rich avifauna in Iran, only a two studies on infestation with lice in great- small number of studies have been conducted white pelican (Pelecanus onocrotalus) and six 63

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wild bird species in Iran (Tavassoli et al., 2011; captured birds were examined for lice Dik and Halajian, 2013). The aim of this study infestation and other ectoparasites. Visual was to identify lice species of passerine birds in examination was the main method for East of Iran. determining infestation by lice, but in some cases post-mortem-ruffling was used. In live Material and methods birds, the lice were detached by delicate brush and transferred to a glass tube containing 70% Sampling was performed from March 2011 ethanol. The lice were mounted in the lab through January 2012 in East of Iran. This area according to the methodology described by is located between 30°21'-38°17'N latitude and Palma (1978). 55°28'-61°20'E longitude and is more than 303,513 square kilometers wide (figure 1). Identification of lice to species level (in some individuals) was done by microscopy using the Mist nets were used for capturing birds at 11 relevant literature. different localities of the study area. The

Figure 1. The study area and sampling localities

Results Menoponidae and Ricinidae were identified only to genus level. During the field study a total of 106 passerine birds of 37 species were captured and examined Menoponidae: Myrsidea spp. Waterston, 1915 for lice infestation (table 1). Fifty two (49.05%) was found on European Green finch ( Carduelis of 106 examined birds were infested. Overall, chloris ). Menachantus spp. Neumann, 1912 465 lice were collected from infested birds another member of this family was detached including 214 females, 90 males and 161 form Common Chiffchaff (Phylloscopus nymphs (table 2). Parasitological studies collybita), Green Warbler (P. nitidus), Lesser revealed that collected lice belonged to three Short-toed Lark (Calandrella rufescens) and Red- Families: Ricinidae, Menoponidae and headed Bunting (Emberiza bruniceps). Philopteridae. Lice belonging to the families 64

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Table 1. Number of examined birds from each species

Number of Number of Bird family Bird Genus Bird species examined birds infested birds Turdidae Turdus Turdus merula 4 1 Luscinia Luscinia megarhynchos 2 1 Saxicola Saxicola torquata 2 1 Oenanthe Oenanthe lugens 2 2 O. alboniger 2 - O. pleschanka 2 - O. picata 2 - Fringillidae Carduelis Carduelis cannabina 2 - C. chloris 2 2 C. obsoleta 2 2 Fringilla Fringilla coelebs 3 2 Paridae Parus Parus major 9 4 P. bokharensis 1 - Muscicapidae Ficedula Ficedula parva 4 - F. striata 3 - Sylviidae Hippolais Hippolais pallida 7 - H. caligata 3 - Acrocephalus Acrocepha lus stentoreus 1 1 A. agricola 1 - Phylloscopus Phylloscopus collybita 11 5 P. nitidus 2 1 Sylvia Sylvia mystacea 2 - S. communis 1 1 Scotocerca Scotocerca inquieta 1 - Passeridae Passer Passer montanus 8 7 P. domesticus 9 9 Petronia Petronia petronia 2 2 P. xanthocollis 1 1 P. brachydactyla 1 - Alaudidae Galerida Galerida cristata 2 1 Calandrella Calandrella rufescens 2 2 Sturnidae Sturnus Sturnus vulgaris 1 1 Acridotheres Acridotheres Tristis 1 1 Emberizidae Emberiza Emberiza bruniceps 3 2 E. calandra 3 2 Sittidae Sitta Sitta neumayer 1 - Corvidae Corvus Corvus corone 1 1 11 Families 22 Genera 37 Species 106 52

Table 2. List of examined birds and their related lice

Hosts N Ni Chewing lice ♂ ♀ n T MI Turdus merula 4 1 Ricinus sp. - 4 - 4 4.00 Saxicola torquata 2 1 Brueelia sp. - 1 1 2 2.00 Luscinia megarhynchos 2 1 Brueelia sp. - 1 - 1 1.00 Oenanthe lugens 2 2 Philopterus sp. 6 - 18 24 12.0 O. alboniger 2 ------O. pleschanka 2 ------O. picata 2 ------Carduelis cannabina 2 ------C. chloris 2 2 Myrsidea sp. - 9 3 12 6.00 C. obsoleta 2 2 Philopterus sp. 3 9 8 20 10.0 2 Brueelia gobiensis 2 15 6 23 11.5 Fringilla coelebs 3 2 Brueelia sp. - 5 7 12 6.0 0 1 Philopterus fringillae - 2 1 3 3.00 65

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Table 2. List of examined birds and their related lice (cont.)

Hosts N Ni Chewing lice ♂ ♀ n T MI Parus major 9 4 Philopterus pallescens 3 1 - 4 1.00 P. bokharensis 1 ------Ficedula parva 4 ------Emberiza calandrela 3 ------Hippolais pallida 7 ------H. caligata 3 ------Acrocephalus stentoreus 1 1 Brueelia sp. - 1 1 2 2.00 A. agricola 1 ------Phylloscopus collybita 11 2 Brueelia sp. 5 16 - 21 10.5 2 Sturnidoecus sp. 8 - 1 9 4.50 2 Philopterus sp. 1 3 6 10 5.00 1 Menacanthus sp. - 1 - 1 1.00 Ph.nitidus 2 1 Brueelia sp. 2 - - 2 2.00 1 Menachantus sp. - 3 6 9 9.00 Sylvia mystacea 2 ------Scotocerca inquieta 1 ------Sylvia communis 1 1 Sturnidoecus sp. 1 - 1 2 2.00 Passer montanus 8 3 Sturnidoecus ruficeps 6 17 - 23 7.60 1 Unknown Genus 5 - - 5 5.00 1 Philopterus montani - 1 - 1 1.00 3 Brueelia subtillis 2 12 - 14 4.60 1 Campanulotes compar - 2 - 2 2.00 Passer domesticus 9 5 Brueelia subtilis 5 15 14 34 6.80 8 Sturnidoecus refractariolus 8 17 9 34 4.25 1 Philopterus fringillae 1 6 12 19 19.00 1 Unknown Genus - 2 - 2 2.00 Petronia petronia 2 1 Brueelia sp. 2 1 - 3 3.00 1 Sturnidoecus refractariolus - 7 - 7 7.00 1 Philopterus sp. - 1 - 1 1.00 Petronia xanthocollis 1 1 Philopterus fringillae 1 1 - 2 2.00 Petronia brachydactyla 1 ------Galerida cristata 2 1 Brueelia sp. 1 3 - 4 4.00 1 Ricinus sp. - 3 - 3 3.00 Calandrella rufescens 2 2 Menacanthus sp. 2 - - 2 1.00 Sturnus vulgaris 1 1 Brueelia nebulosa 20 41 57 118 118.0 Acridotheres tristis 1 1 Brueelia chayanh 2 2 2 6 6.00 Emberiza bruniceps 3 1 Menacanthus sp. - 1 - 1 1.00 2 Sturnidoecus rostratus 3 5 5 13 6.50 Emberiza calandra 3 1 Brueelia sp. 1 1 - 2 2.00 2 Sturnidoecus rostratus - 4 3 7 3.50 Sitta neumayer 1 ------Corvus corone 1 1 Brueelia sp. - 1 - 1 1.00 106 - - 90 214 161 465 N = number of examined birds; Ni = number of infested birds; n = nymph; T = total number; MI = mean intensity; Mean intensity = no. of lice/no. infested birds.

Ricinidae: Ricinus spp. DeGeer, 1778 was found Sparrow (P. montanus), B. gobiensis Mey, 1982 on Common Blackbird (Turdus merula) and from Desert Finch (Carduelis obsoleta), Crested Lark (Glerida cristata). Philopterus pallescens Denny, 1842 on Great Tit (Parus major), P. montani Zlotorzycka, 1964 and Philopteridae: Eleven species were identified as Campanulotes compar Keler, 1939 on Tree follow: Brueelia chayanh Ansari, 1955 on Sparrow , P. fringillae Scopoli, 1772 on Common Common Myna (Acridotheres tristis), B. nebulosa Chaffinch (Fringilla coelebs), House Sparrow and Burmeister,1838 from Common Starling Chestnut-shouldered Petronia (Petronia (Sturnus vulgaris), B. subtilis Nitzsch, 1874 on xanthocollis), Sturnidoecus refractariolus House Sparrow (Passer domesticus) and Tree Zlotorzycka, 1964 on House Sparrow and 66

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Common Rock-sparrow (Petronia petronia), S. B. chayanh was detached from Common Myna in ruficeps Nitzsch, 1866 on Tree Sparrow and this study. Saxena et al. (2007) and Ansari finally S. rostratus Mey, 1982 on Corn Bunting (1957) has reported this louse species on (Emberiza calandra) and Red-headed Bunting. Common Myna from India and Pakistan, There were some individuals in these four respectively. mentioned genus that were not identified to the species level. Reporting of S. ruficeps on Tree Sparrow and S. refractariolus on House Sparrow and Common Discussion Rock-sparrow in this study is in agreement with Adam et al. (2009) findings from Romania. In Iran, only a few studies have been conducted on lice infestation in wild birds. There was no S. rostratus have been reported on Red-headed previous targeted research on lice infestation of Bunting and Corn Bunting in USA and Bulgaria, passerine birds. We report for the first time in respectively (Dalgleish, 2003; Lieva, 2009). In this study lice on 37 passerine bird species the current study, we have also found infesting examined. Below we present details on our these two species. findings. C. compar was detected on Tree Sparrow in the P. pallescens was found on Great Tit in this current study. According to reports of Price et study. Lieva (2009) has reported this louse from al. (2000), Galloway and Palma (2008), Lieva Great Tit in Bulgaria. (2009), and Naz et al. (2010) Columba livia is the normal host of this louse species. There is no P. fringillae has been found on Common previous report about infestation of passerine Chaffinch and House Sparrow in Russia, birds with this species and we speculate that Romania, Pakistan, Bulgaria and Arizona cross-infestation was the cause for this finding. (Ansari, 1957; Mayberry et al., 2000; Rekasi and Kiss, 2006; Lieva, 2009; Lyakhova and Kotti, There were a number of lice specimens that we 2011). In the current study this species was were not able to identify to the species level. found on three hosts including Common Lack of reliable identification keys and/or Chaffinch, House Sparrow and Chestnut- existence of only one sex and/or lack of access shouldered Petronia. There is no previous to adult stages for some species were the causes record of this species on Chestnut-shouldered for this situation. One specimen was not Petronia. identified to the genus level and is still under study. Adam et al. (2009) have reported P. montani from Tree Sparrow in Romania. This species The results of this study lists seven genera and was found on mentioned host in the study area. 11 species of chewing lice on 24 species of We report for the first time the lice B. gobiensis passerine birds in Iran. Identified lice species in on Desert Finch in this study. B. subtilis has been the current study were recorded for the first found on Tree Sparrow (P. montanous), House time in Iran. It is recommended that more Sparrow and Common Chaffinch in this study. studies should target ectoparasite fauna of wild This louse has been reported on Tree Sparrow birds in other areas of Iran. and House Sparrow in Arizona, Bulgaria and Pakistan (Mayberry et al., 2000; Lieva, 2009; Acknowledgements Ansari, 1957). Finding of B. subtilis on Common Chaffinch in this study is also the report for a We thank Dr. A.H. Fallah-Rad for editing the new host. manuscript and Dr. Sara Bush for her collaboration in this project. We would like to We also found B. nebulosa on Common Starling thank Ferdowsi University of Mashhad for which had been reported on this host in providing the financial support for this study. Romania, Turkey and Arizona (Mayberry et al., 2000; Adam et al., 2009; Dik et al., 2011).

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