Journal of the Egyptian Society of Parasitology, Vol.42, No.3, December 2012 J. Egypt. Soc. Parasitol., 42(3), 2012: 525 – 533 FIRST RECORDS OF THE CHEWING LICE (PHTHIRAPTERA) ASSOCI- ATED WITH EUROPEAN BEE EATER (MEROPS APIASTER) IN SAUDI ARABIA By AZZAM EL-AHMED1, MOHAMED GAMAL EL-DEN NASSER1,4, MOHAMMED SHOBRAK2 AND BILAL DIK3 Department of Plant Protection1, College of Food and Agriculture Science, King Saud University, Riyadh, Department of Biology2, Science College, Ta'if University, Ta'if, Saudi Arabia, and Department of Parasitology3, Col- lege of Veterinary Medicine, University of Selçuk, Alaaddin Keykubat Kampüsü, TR-42075 Konya, Turkey. 4Corresponding author: [email protected], [email protected] Abstract The European bee-eater (Merops apiaster) migrates through Saudi Arabia annu- ally. A total of 25 individuals of this species were captured from three localities in Riyadh and Ta'if. Three species of chewing lice were identified from these birds and newly added to list of Saudi Arabia parasitic lice fauna from 160 lice individu- als, Meromenopon meropis of suborder Amblycera, Brueelia apiastri and Mero- poecus meropis of suborder Ischnocera. The characteristic feature, identification keys, data on the material examined, synonyms, photo, type and type locality are provide to each species. Key words: Chewing lice, Amblycera, Ischnocera, European bee-eater, Merops apiaster, Saudi Arabia.

Introduction As the chewing lice species diversity is Few studies are available on the bird correlated with the bird diversity, the lice of migratory and resident birds of Phthiraptera fauna of Saudi Arabia ex- the Middle East. Hafez and Madbouly pected to be high as at least 444 wild (1965, 1968 a, b) listed some of the species of birds both resident and mi- chewing lice of wild and domestic gratory have been recorded from Saudi birds of Egypt. Three papers have re- Arabia Kingdom (Silsbee, 1980; Ano- ported on the chewing lice of domesti- nymous, 2005; Al-Yusef; 2006). The cated fowl in the Kingdom of Saudi majority of these birds have affinities Arabia (Abu Yaman, 1978; Aldryhim, with neighboring regions reflecting the 1991; Taula and Hussain, 1999), but importance of understanding the chew- none on the chewing lice of wild birds. ing lice fauna of the Saudi Arabia.

525 The European bee-eater Merops api- search Unit at Dirab [24o24'31.34''N, aster Linnaeus is a migratory insectivo- 46o39'36.21''E]) (Fig 1), Also. on the rous bird which breeds in southern Eu- National Wildlife Research Center near rope, in some parts of North Africa and Ta'if [21o 15'1''N, 40o 32'42'']. Live col- western Asia (Snow 1978).This species lected birds were carefully examined occurs in Saudi Arabia as migrant bird visually and any lice removed using that travels through the kingdom during forceps. its annual flight (Stagg, 1994). Migra- The bird were then placed in a fumi- tion is in the form of small groups that gation chamber using chloroform to can be easily detected around the apiar- kill remaining lice and then combed for ies where it may cause the economical removing the rest (Fig 2). The exam- losses in honey production either due ined birds were released in the same to feeding on worker honey bees or locality of capture. The collected lice restricting of bee foraging behavior were placed in 70% ethyl alcohol then (Pokhrel 2008, Alfallah et al, 2010). selected specimens were transferred to Much has been published on chewing lactic acid for two days for clearing and lice associated with the European bee- then mounted on microscopic slides eater (Price and Emerson 1977, Wil- using Puri's Media. All specimens were liams 1981, Adam 2004, Kri-stofík et photographed using a Nikon DS-Fi1 al, 2006, Adam et al, 2009), but did not camera12mp fixed on Nikon micro- mention the made of any records from scope eclipse 80i. Photoshop CS4 was Saudi Arabia. used to prepare final images. No taxonomic keys are available for The lice identifications were done the chewing lice infesting the European using Bienko (1964), Price and Emer- bee-eater. The objective of this study is son (1977), Williams (1981), and Ad- to update the knowledge of chewing am (2004). The specimens were depos- lice associated with M. apiaster, report- ited in the Plant Protection Department ing on the lice species collected from (CPPD), King Saud University, Ri- this bird in Saudi Arabia and provided yadh, the symbols used are (F) for fe- an identification key for them. male, (M) for male and (N) for nymph. Material and Methods Results A total number of 160 chewing lice Birds were collected using standard specimens were collected from 23 of mist nets (mesh: 1.8cm x 0.12mm & 25 total birds captured. Three species size: 2m x 15m) during their migratory of the chewing lice were identified: period in April and May on 2011 & Brueelia apiastri (Denny, 1842) largest 2012. The nets were placed around api- with 85 individuals, Meropoecus mer- aries at two localities near Riyadh opis (Denny, 1842) with 55 individuals (King Saud University Educational and Meromenopon meropis Clay & Farm west of Riyadh [24o44'11.99''N, Meinertzhagen, 1941 with 20 individu- 46o37'10.30''E] and the Agriculture Re- als. 526 Key to species of chewing lice infested European bee-eater: 1. Maxillary palps present; antennae capitates, 5 segmented, concealed in antennal fossae; preocular slit present usually deep and narrow, hind legs and abdominal sternites with groups of small seta ……………….....Meromenopon meropis (Fig.3) - Maxillary palps absent; Antennae filiform with 5 segments directed backward on the side of head; Preocular slit absent, third legs and abdominal sternites without such groups of setae..……………………………………………………. ………...2 2. Body elongated, head longer than broad; postgenae with one long seta; head with distinct oral groove; carina at anterior margin of head weakly develop- ed..…………………………………………………………Brueelia apiastri (Fig. 4) - Body stout, head broader than long; postgenae enlarged with more than one seta; clypeus with transparent anterior part reaches carina.Meropoecus meropis (Fig.5,6) Suborder: Amblycera Family: Menoponidae Genus: Meromenopon Clay & Meinertzhagen, 1941 Meromenopon meropis Clay & Meinertzhagen, 1941 Tamaninia rara Conci, 1941: 106. Meromenopon concii Tendeiro, 1961: 291. Known hosts: Merops apiaster L. (Type host) & Merops bullock Vieillot (Coracii- formes: Meropidae). Type: Holotype male in the Meinertzhagen Collection. Slide no. 10086. Locality: Afghanistan. This species was collected from ab- a group of small seta in ventral face of domen and under wings plumage. The femur; Abdomen oval in shape, sterni- head is slightly broader than long, oc- tes well sclerotized, from III-VI with cipital border concave with brown two groups of small seta, there is also margin, antennal fossa deep and its rows of marginal seta on the abdominal inner margin dark brown, postocular sternites that increasing laterally form- fringe thick with small hairs becoming ing sterna brushes. posteriorly continuous ending with Material examined (20): Educational longer marginal temporal setae; Pro- farm, west of Riyadh 24. IV.2011 F(5), thorax slightly broader than long well M (0), N(10);National Wild life Re- sclerotized dorsally with 8 marginal search Center 11.V.2012 F(3), M(1), seta; legs concolor, the hind ones with N(1),(CPPD). Suborder: Ischnocera Family: Philopteridae Genus: Brueelia Kéler, 1936 Corvonirmus Eichler, 1944:80. Traihoriella Ansari, 1947:290. Guimarãesiella Eichler, 1949:11. 527 Allobrueelia Eichler, 1951:36. Hirundiniella Carriker, 1963:312. Allonirmus Zlotorzycka, 1964:263. Maculinirmus Zlotorzycka, 1964:247. Brueelia apiastri (Denny, 1842) Nirmus apiastri Denny, 1842:52. Known hosts: Merops apiaster L. (Type host) (Coraciiformes: Meropidae). Type: Holotype damaged "without head" British Museum slide no. 1852.98. Locality: Belfast, Ireland. This species was usually collected tergites usually separated from the from the neck and chest plumage. The middle in both sexes; genitalia of male body dimension of this species usually is in characteristic shape that distin- larger than that of any Brueelia species guished it from any other Brueelia spe- and it characterized by triangular head cies. in outline being interiorly narrower Material examined (85): Agriculture than rest of the head, the middle and Research Unit at Dirab 10.IV.2011 lateral margin of carina interrupted, F(16), M (7), N(9); Educational farm at preantennal nodus small; the posterior west of Riyadh 24. IV.2011 F(8), M(3), lateral angles of prothorax rounded; the N(2); 20. IV.2012 F(10), M(7), N(3); abdominal segments from I-VI with National Wild life Research Center sclerotized lateral margins and its 11.V.2012 F(8), M (3), N(9),(CPPD) Genus: Meropoecus Eichler, 1940 Meropoecus meropis (Denny, 1842) Docophorus meropis Denny, 1842. Docophorus bifrons Nitzsch, 1866:116. In Hopkins & Clay 1952:225. Known hosts: Merops apiaster L. (Type host), Merops persicus persicus Pallas and Merops superciliosus L. (Coraciiformes: Meropidae). Type: British Museum. Locality: Ireland. This species is usually collected from size of head, it show some aspect of the head region and small feathers un- sexual dimorphism between male and der the bill. Head is quadrangular, female as it is rectangular in male and broader than its long, Dorsal preanten- pentagonal in female, the legs unicol- nal suture is well underlined along the orous equal in size; abdomen oval in sides of the dorsal anterior plate and shape with strongly pigmented pleu- the inner side of the marginal carina, rites, the male have characteristic geni- Antennae are filiform with long pedicel talia (Fig.5) and characteristic sperma- that longer than the flagellomeres thecal ring apparent at the posterior which are equal in size; the first thorac- female abdomen (Fig.6). ic segment is very small relative to the

528 Material examined (55): Agriculture parasitic relationship as it usually asso- research unit at Dirab 10.IV.2011 F ciated with bee-eater genera of family (11), M (7), N(5); Educational farm, Meropidae and some species of rollers west of Riyadh. 24. IV.2011 F(5), M of family Coraciidae. The species of (5), N(2), 20.V. 2012 F(4) M(2) N(0); this genus usually show some flexibil- National Wild life Research Center ity in host association but our species is 11.V.2012 F(4) M(6) N(4),(CPPD) only recorded from Merops apiaster L. and M. bullock Vieillot (Price and Em- Discussion erson, 1977). The three species of chewing lice The Suborder Ischnocera was repre- associated with migratory European sented by one family Philopteridae and bee-eater are recorded for the first time two species Brueelia apiastri and Mer- from Saudi Arabia. The density of lice opoecus meropis. Denny (1842) de- relative to the 23 collected birds varied, scribed the two species from the Euro- the most abundant species was B. api- pean bee-eater but in 2 different gene- astri. The plumage condition of all cap- ra. There are five species of Brueelia tured birds was good except for three infesting rollers and bee-eaters around individual that was heavily infested the world but B. apiastri show high with all three lice species and one of degree of host specificity and only rec- them with species of an unidentified orded on the Merops apiaster L. (Wil- hard tick (Ixodidae). Kristofík et al. liams, 1981). Adam (2004) provided (2006) indicated that overall condition extensive information on M. meropis of plumage and bill length of bee-eater from birds collected in Romania. This effect greatly the lice population on the species also forms a type of the genus bird plumage and this compatible with Meropoecus which described by Eich- our case. The lower number of Mer- ler (1940). M. meropis has a wide omenopon meropis may be due to sea- range of Coraciiformes hosts and may sonality development phenology or the be transferred to resident species of low sample size. Most of individuals of bee-eaters such as Little Green Bee- this species were nymphs indicating eater Merops orientalis Latham 1802 maturity will occur in the summer after by migratory species, but more work the bird returns to Europe, some works are needed to confirm this phenomena. on the same bird in Europe collected only this species (Dik et al, 2011). Conclusion This is the first contribution to chew- From a taxonomic point of view, two ing lice associated with wild birds of suborder of chewing lice are represent- Saudi Arabia. Additional studies to ed in lice associated with European survey bird lice fauna of resident and bee-eater. M. meropis is a member of migratory birds in the Kingdom, espe- suborder Amblycera and family Meno- cially for endemic and endangered ponidae is the type of genus Merome- birds are ongoing and will be published nopon. This genus is very specific in its in due time else-where. 529 tional d'Histoire Naturelle, Grigore An- Acknowledgment tipa 47:129-37. This work was supported by King Saud University, Deanship of Scientific Adam, C, Chsamera, G, Daróczi, SJ, Research and College of Food and Ag- Sándor AD, Gogu-Bogdan, M, 2009: riculture Science Research Center so Data on the chewing louse fauna (Phth- the authors are gracefully thank for iraptera: Amblycera, Ischnocera) from their kind support and help. some Wild and Domestic birds of Ro- mania. Travaux du Muséum National The authors would like to thank the d’Histoire Naturelle, 52:177-232. Saudi Wildlife Committee for support- ing this study and accepted to deal and Aldryhim, Y, 1991: Mallophaga of the handle wild birds in many protected domestic chicken in the central region areas and special thanks and grateful- of Saudi Arabia. Emir. J. Agric. Sci. 3: ness goes to his excellency the Prince 143-50. Bander Bin Saud Bin Mohammad, the Alfallah, HM, Alfituri, M, Hmuda, President of Saudi Wildlife Authority M, 2010: The impact of bee-eater Mer- for his sponsorship of the study of ops apiaster on the behavior of honey chewing life associated with wild birds bee Apis mellifera during foraging. J. of Saudi Arabia. Plant Protect. Pathol. Mansoura Uni- Great appreciations are due to Prof. versity 1, 12:1023-34. Boris Kondratieff, Colorado State Uni- Alyousef, MS, 2006: Wild and Migra- versity, Fort-Collins, Colorado, USA tory birds of Saudi Arabia. Dar El-Bah- for assistance in linguistics of the man- use Publisher: Riyadh, Saudi Arabia. uscript. Anonymous 2005: The National Strat- Furthermore the authors are thankful egy for Conservation of Biodiversity in to Mr. Mohamed F. Sallam from Chair the Kingdom of Saudi Arabia. National of Insect Vector Born Disease and Col- Commission for Wildlife Conservation leges in Chair of Engineer Abdullah and Development, 19-20. Bagshan for Bee Research for their Bienko, GB, 1964: Keys to the Insects kind help during the study. of the European USSR: Apterygota, Palaeoptera, Hemimetabola. Israel Pro- References gram for Scientific Translations 1:385- Abu Yaman, IK, 1978: Insects and 402. other pests affecting man and animals Clay, T, Meinertzhagen, R, 1941: in Saudi Arabia. Angew. Parasitol. 19: Mallophaga miscellany, No. 2. Ann. 31-3. Magaz. Nat. Hist. (Ser. 11), 7:329-346 Adam, C, 2004: Some morphological Denny, H, 1842: Monographia anoplu- aspects in the species Meropoecus rorum Britanniae or an Essay on the meropis (Denny, 1842) (Phthiraptera: British Species of Parasitic Insects, Ischnocera). Travaux du Muséum Na- Henry G. Bohn

530 Dik, B, Şekercioğlu ÇH, Kirpik MA, rops apiaster). Parasitol. 134, 3:399- 2011: Chewing lice (Phthiraptera) spe- 403. cies found on birds along the Aras Riv- Pokhrel, S, 2008: The ecological prob- er, Iğdır, East. Turkey. Kafkas Univ. lems and possible solutions of beekeep- Vet. Fak. Derg. 17, 4:567-73. ing in hills and terai of Chitwan, Nepal. Eichler, W, 1940: Notulae Mallopha- J. Agricul. Environ. 9:23-33. gologicae. IV- Neue Gattungen und hö- Price, RD, Emerson. KC, 1977: The here Einheiten von Kletterfederlingen. genus Meromenopon (Mallophaga: Zool. Anzeiger 130, 5/6:97-103. Menoponidae) from the Coraciiformes Hafez, M, Madbouly MH, 1965: Bird (Aves). J. Kansas Entomol. Soc. 50, 2: lice infested domestic birds in Egypt. 215-21. Bull. Soc. Entomol. d'Egypte 10:181- Silsby, JD, 1980: Inland Birds of Sau- 213. di Arabia. Immel, London. Hafez, M, Madbouly MH, 1968a: Snow, W, 1978: Relationships bet- Mallophaga infesting migratory birds ween the European and African Avi- in Egypt. Bull. Soc. Entomol. d'Egypte, fauna. Bird Study 25, 3:134-48. 52:113-54. Stagg, A, 1994: Birds of the Riyadh Hafez, M, Madbouly MH, 1968b: Region: an Annotated Checklist. SWC, Mallophaga infesting resident birds in Riyadh, KSA. Egypt. Bull. Soc. Entomol. d'Egypte Taula, FH, Hussain, H, 1999: Study 52:53-111. on the seasonal incidence of chewing Hopkins, GHE, Clay, T, 1952: A Ch- lice in the western region (Jeddah) eck List of Genera & Species of Mal- (Mallophaga) on pigeons and turkeys lophaga; British Museum of Natural in Saudi Arabia. Saudi J. Biol. Sci. 6, History, London. 2:3-13. Kristofík, J, Darolová, A, Hoi, C, Williams, NS, 1981: The Brueelia Hoi, H, 2006: Determinants of popula- (Mallophaga, Philopteridae) of the Me- tion biology of the chewing louse ropidae (Aves, Coraciiformes). J. Kan- Brueelia apiastri (Mallophaga, Philopt- sas Entomol. Soci. 54, 3:510-8. eridae) on the European bee-eater (Me-

531 Fig.1: Migratory European bee-eater captured by mist net screened around the apiary of Agriculture Research Unit at Dirab, Saudi Arabia.

Fig.2: European bee-eater on fumigation chamber containing cotton filled with 95% chloroform to kill all lice.

532 Fig. 3: Female Meromenopon meropis Clay & Meinertzhagen, Fig.4: Female Brueelia apiastri (Denny), Fig. 5: Male Meropoecus meropis (Denny) and Fig. 6: Female Meropoecus meropis (Denny).

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