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Home , African fish eagle, Amblycera, Augur buzzard, Bateleur, Black eagle, Butastur

An analysis of /chewing lice interaction, with a new record for Saudi Arabia

§ M. Nasser1 , A. Alahmed2, M. Ansari2 , E. Adly1* & M. Shobrak3 1Department of Entomology, Faculty of Science, Ain Shams University, Cairo, Egypt 2Department of Botany, Hindu College, Moradabad, 244001, 3Department of Biology, Science College, Ta’if University, Ta’if, Saudi Arabia

Parasitism is a hostile relationship that helps greatly in the development and evolution of many creatures in their race for survival. Chewing lice of nestlings of the osprey Pandion haliaetus (L.) have been studied in Farasan Island, Saudi Arabia. All previous chewing lice re- cords from this have also been reviewed. Four of chewing lice are previously known to infest P. haliaetus. The nestlings of the osprey in Farasan were only infested by Colpocephalum turbinatum Denny, 1842. This species of chewing lice is recorded herein for the first time from the Kingdom of Saudi Arabia and its distributional pattern is very characteris- tic among three different avian orders (, Columbiformes, and Strigiformes). Colpocephalum turbinatum was found mainly on terrestrial of the Columbiformes and it may be transferred to predatory birds in the other two orders, but the presence of this parasite on some aquatic birds of prey like osprey may indicate that the ancestors of these birds were terrestrial hunters that acquired this from their prey such as doves and pigeons before their transference to aquatic life. The pattern of chewing lice distribution through their host populations and habitats may reveal some important ecological and evo- lutionary events that happened to their hosts in the past. Key words: Colpocephalum turbinatum Denny, 1842, Pandion haliaetus (L.), Saudi Arabia, birds of prey.

INTRODUCTION

Half of surrounding is parasitic importance to understand their relationship with creatures (Hannah & Lovejoy 2003). So, the role their host birds. that these organisms play in evolution and devel- Osprey, Pandion haliaetus (L.), is a common marine opment of the life on earth is impressive. Chewing -eating . It is one of the most widely lice are such parasites that can invade spread birds of prey on the planet. Its range and bird’s bodies for food and shelter, with about extends to all continents except Antarctica and it is 4000 species worldwide. They form one of the found in temperate and tropical regions, espe- most diversified groups of parasitic in the cially oceans, sea coasts and sometimes in fresh- global fauna (Imms et al. 1977; Price et al. 2003). As water habitats (Alderton 2008). In Saudi Arabia, permanent, slow-moving ectoparasites, chewing the osprey is a resident breeding sea bird that is lice show some degree of host specificity that found along the coast of the Red Sea and some allow them to act as a clue in studying host/para- islands of the Gulf (Jennings 2010; Shobrak & site phylogeny and coevolution (Hopkins 1941; Aloufi 2014). Banks & Paterson 2004). Four species of lice are known to infest osprey, all The chewing lice of marine birds is a very inter- of them belonging to the suborder : esting group of insects which have been neglected Colpocephalum napiforme Rudow, 1869, Colpo- for a long period in several parts of the world, cephalum turbinatum Denny, 1842 and Kurodaia especially in the Middle East (Negm et al. 2013). haliaeeti (Denny, 1842) of the family , Recently, these creatures drew the attention of and Laemobothrion maximum (Scopoli, 1763) of entomologists and marine biologists all over the family . Only K. haliaeeti is the world (Banks & Palma 2003; Palma 2012; specific to osprey, while the other three species are Al-Ahmed et al. 2014), and this may be due to the known from related and non-related bird hosts

*Author for correspondence. E-mail: [email protected] / [email protected]

Received 17 July 2018. Accepted 16 November 2018

ISSN 1021-3589 [Print]; 2224-8854 [Online] African Entomology 27(1): 178–184 (2019) DOI: https://doi.org/10.4001/003.027.0178 ©Entomological Society of Southern Nasser et al.: An analysis of osprey/chewing lice interaction with a new record for Saudi Arabia 179

(Price et al. 2003). Only a few cases of osprey/chew- urubitinga (Gmelin); Osprey, Pandion ing lice interaction are known (Miller et al. 1997) so haliaetus (L.); Slender-billed , Rostrhamus the aim of this work is to analyse the relationship hamatus (Temminck); African Fish , between this bird and its associated chewing lice. Haliaeetus vocifer (Daudin); Grey-headed fish Also, to record the chewing louse Colpocephalum eagle, Ichthyophaga ichthyaetus (Horsfield); African turbinatum in Saudi Arabia for the first time. -, Polyboroides typus Smith; Madagas- can harrier-hawk, Polyboroides radiatus (Scopoli); MATERIAL AND METHODS hawk, Buteogallus meridionalis (Latham); As a part of an extensive study on the chewing Red-shouldered hawk, lineatus (Gmelin); lice fauna of wild birds in Saudi Arabia, we Red-tailed hawk, Buteo jamaicensis (Gmelin); checked the breeding population of nestlings Crested eagle, Morphnus guianensis (Daudin); of osprey on Farasan Island, Kingdom of Saudi Harpy eagle, Harpia harpyja (L.). Arabia on 6 February 2015 (16°46’43”N 41°59’17”E). This species is characterised by a very long Farasan forms the largest marine protected island mid-dorsal head seta, marginal prothorax with of archipelago in the Red Sea, which has a long hot four long and two short setae, abdomen without season from April to October, with average annual row of anterior setae along tergites. This species temperature of 30 °C and RH 65 % to 80 %. One recorded as a potential parasite of osprey on the nest with two juvenile birds was examined for latest world checklist of chewing lice (Price et al. chewing lice. The bird handling occurred with 2003). permission of the Saudi Wildlife Authority. Lice were collected by visual inspection of host feathers Colpocephalum turbinatum Denny 1842, and were preserved on 95 % alcohol. Slides were Fig. 1 prepared using Puri’s media. The lice identifica- Colpocephalum ailurum Nitzsch (in Giebel), 1861 tions were done using Price et al. (2003) and Naz Colpocephalum bicinctum Nitzsch (in Giebel), et al. (2012). All previous records of chewing lice 1861 from osprey were also revised and reviewed Colpocephalum caudatum Giebel, 1874 (Eichler 1941; Clay & Hopkins 1951; Price & Beer Colpocephalum dissimile Piaget, 1880 1963a, b; Nelson & Price 1965; Miller et al. 1997; Colpocephalum intermedium Piaget, 1880 Price et al. 2003). These data were analysed to show Colpocephalum costaricense Carriker, 1903 the specificity of chewing lice infesting osprey and Colpocephaluma bruptofasciatum Mjöberg, 1910 try to answer how species such as Colpocephalum Neocolpocephalum wetzeli Eichler, 1941 turbinatum transferred to such a marine bird of Colpocephalum wernecki Orfila, 1959 prey. Also, the latest evolutionary studies of Known hosts. (type host), Columba livia marine birds of prey were screened to help us Gmelin; Pied imperial-pigeon, Ducula bicolor answer this question (Lerner & Mindell 2005). The (Scopoli); White-winged dove, Zenaida asiatica (L.); material collected is deposited in the King Saud White-tailed kite, Elanus leucurus (Vieillot); Brah- University Museum of (KSMA). miny kite, indus (Boddaert); Whistling kite, Haliastur sphenurus (Vieillot); Black kite, RESULTS migrans (Boddaert); Red kite, Milvus milvus Four species of chewing lice (three in the family (L.); , Terathopiusecaudatus (Daudin); West- Menoponidae and one in the family Laemoboth- ern marsh harrier, Circus aeruginosus (L.); Spotted riidae) have in the past been recorded on osprey. harrier, Circus assimilis Jardine & Selby; Swamp Only one out of the four species is recorded for the harrier, Circus approximans Peale; Northern har- first time here from Saudi Arabia. rier/hen harrier, Circus cyaneus (L.); Brown gos- hawk, fasciatus (Vigors & Horsfield); Suborder Amblycera African goshawk, Accipiter tachiro (Daudin); Dark Family Menoponidae chanting goshawk, Melierax metabates Heuglin; : Colpocephalum Nitzsch, 1818 , Buteo galapagoensis (Gould); Red-tailed hawk, Buteo jamaicensis (Gmelin); Colpocephalum napiforme Rudow, 1869 , Buteo magnirostris (Gmelin); Colpocephalum heterospizium Carriker, 1963 Swainson’s hawk, Buteo swainsoni Bonaparte; Known hosts.Greatblackhawk(typehost), Prairie , Falco mexicanus Schlegel; Wedge- 180 African Entomology Vol. 27, No. 1, 2019

Fig. 1. Female Colpocephalum turbinatum Denny 1842 with a drawing of male genitalia to the right. tailed eagle, audax (Latham); , Cape griffon, coprotheres (Forster); Griffon Haliaeetus leucocephalus (L.); White-bellied sea , Gyps fulvus (Hablizl); , Gyps eagle, Haliaeetus leucogaster (Gmelin); Pallas’s fish indicus (Scopoli); Ruppell’s griffon, Gyps rueppellii eagle, Haliaeetus leucoryphus (Pallas); African fish (Brehm); , Necrosyrtes monachus eagle, Haliaeetus vocifer (Daudin); Little eagle, (Temminck); , Neophron percno- Hieraaetus morphnoides (Gould); Booted eagle, pterus (L.). Hieraaetus pennatus (Gmelin); Long-crested eagle, Remarks. This species was collected from fluffy Lophaetus occipitalis (Daudin); , feathers on the abdomen of juvenile osprey. Polemaetus bellicosus (Daudin); Mountain hawk- Head smoky brown with six pitchy dark spots eagle, Spizaetus nipalensis (Hodgson); Eurasian with frontal pair small, antenna not completely , Buteo buteo (L.); , Buteo covered, palpi and antennae protruding espe- rufofuscus (Forster); Long-tailed buzzard, Henico- cially apical segment, pre-antennal margin with longicauda (Garnot); Laughing falcon, six setae, three of them slightly longer, temple Herpetotheresca chinnans (L.); Osprey, Pandion rounded with numerous small setae; thorax with haliaetus (L.); , Pernisa characteristic shape, prothorax rhombus with two pivorus (L.); Oriental honey buzzard, Pernisptilo posterior setae on each side and clear large coxa, rhyncus (Temminck); Barred eagle-, Bubo med and metathorax somewhat triangular with a sumatranus (Raffles); Brown fish-owl, Ketupa spinelike seta in the middle, legs equal in length, zeylonensis (Gmelin); Barking owl, Ninox connivens marginal bands of all legs paler than any other (Latham); Barn owl, Tyto alba (Scopoli); Cinereous species in the genus, fore legs with enlarged tibia, vulture, Aegypius monachus (L.); African white- hind femora with three clear spiny combs on backed vulture, Gyps africanus Salvadori; Indian ventral side; abdomen elongated in female, white-backed vulture, Gyps bengalensis (Gmelin); rounded in male, characterised by faint lateral Nasser et al.: An analysis of osprey/chewing lice interaction with a new record for Saudi Arabia 181 spots on widest segments I and II, large patchy vocifer (Daudin); Grey-headed fish eagle, Ichthyo- dark spots appear from III segment to VII, lateral phaga ichthyaetus (Horsfield); Short-toed eagle, setae appear through the abdominal segment gallicus (Gmelin); Brown eagle, ending in female with tuft-like lateral hairs on Circaetus cinereus Vieillot; Western marsh harrier, segment IX, the posterior margin of sternum of Circus aeruginosus (L.); Swamp harrier, Circus segment IX with a row of bristle-like setae, abdom- approximans Peale; Northern harrier/hen harrier, inal tip rounded in female with two long setae and Circus cyaneus (L.); Montagu’s harrier, Circus two small spines, in male genitalia with very small pygargus (L.); African harrier-hawk, Polyboroides parameres. This species was recorded as a poten- typus Smith; Madagascan harrier-hawk, Poly- tial parasite of osprey in the world checklist of lice boroides radiatus (Scopoli); Dark chanting gos- (Price et al. 2003). hawk, Melierax metabates Heuglin; Pale chanting Material examined (1). Pandion haliaetus (L.): 1 , goshawk, Melierax canorus (Thunberg); Shikra, 9 6 Feb. 2015. Accipiter badius (Gmelin); Levant sparrow hawk, Measurements. Head length 0.3 mm; head widest Accipiter brevipes (Severtzov); Cooper’s hawk, 0.47 mm; head index 0.64 mm; thorax length Accipiter cooperii (Bonaparte); Black sparrow hawk, 0.33 mm; abdomen length 1.17 mm; total length Accipiter melanoleucus Smith; , 1.8± 0.2 mm. Accipiter gentilis (L.); White-eyed buzzard, teesa (Franklin); Grey-faced buzzard, Butastur Kurodaia haliaeeti (Denny, 1842) indicus (Gmelin); Harris’s hawk, uni- Colpocephalum haliaeeti Denny, 1842 cinctus (Temminck); Black-collared hawk, Colpocephalum pachygaster Giebel, 1874. Busarellus nigricollis (Latham); Roadside hawk, Known hosts.Osprey(Typehost)Pandion Buteo magnirostris (Gmelin); Swainson’s hawk, haliaetus (L.). Buteo swainsoni Bonaparte; Red-tailed hawk, Buteo This species is specific to osprey and has never jamaicensis (Gmelin); Long-legged buzzard, Buteo recorded from any other hosts. It can be easily rufinus (Cretzschmar); , Buteo distinguished from any other species in the genus regalis (Gray); Rough-legged buzzard, Buteo Kurodaia by the weakly developed hypopharyn- lagopus (Pontoppidan); , Buteo geal sclerite, characteristic chaetotaxy of female augur (Ruppell); Jackal buzzard, Buteo rufofuscus terminalia and unique male genitalia with wide (Forster); Indian black eagle, Ictinaetus malayensis flattened structure. This is the most common (Temminck); , Aquila rapax species in the genus, with a large number of (Temminck); , Aquila chrysaetos (L.); individuals having been collected from osprey, Verreaux’s eagle, Aquila verreauxii Lesson; especially from North America (Price & Beer Wahlberg’s eagle, Hieraaetus wahlbergi 1963a). (Sundevall); Bonelli’s eagle, Hieraaetus fasciatus (Vieillot); Booted eagle, Hieraaetus pennatus Family Laemobothriidae (Gmelin); Little eagle, Hieraaetus morphnoides Genus Laemobothrion Nitzsch, 1818 (Gould); Martial eagle, Polemaetus bellicosus (Daudin). Laemobothrion maximum (Scopoli, 1763) Laemobothrion maximum is the type species of the Pediculus maximus Scopoli, 1763 genus Laemobothrion. This genus was erected by Laemobothrion giganteum Nitzsch, 1818 Nitzsch when he examined samples of this species Known hosts. Eurasian buzzard (Type host), Buteo giving it a new name Laemobothrion giganteum buteo (L.); Pacific baza, subcristata (Gould); Nitzsch, 1818. The new name of Nitzsch was Osprey, Pandion haliaetus (L.); Hook-billed kite, synonymised by Clay & Hopkins (1951). Eichler Chondrohierax uncinatus (Temminck); European (1941) provided a very good photograph for this honey buzzard, Pernis apivorus (L.); Mississippi species and designated a neotype. The first record kite, Ictinia mississippiensis (Wilson); Red kite, of this species from osprey was by Nelson & Price Milvus milvus (L.); Black kite, Milvus migrans (1965) from samples collected in North America. (Boddaert); Whistling kite, Haliastur sphenurus Laemobothrion maximum is characterised by the (Vieillot); , Haliastur indus very large body, characteristic hypopharyngeal (Boddaert); White-bellied , Haliaeetus sclerite and unique, very simple male genital leucogaster (Gmelin); African fish eagle, Haliaeetus structure with mace shape. 182 African Entomology Vol. 27, No. 1, 2019

DISCUSSION formes to the terrestrial common ancestor of Acciptridae group several millions of years ago The chewing lice/osprey interaction forms a (Fig. 2). The most interesting point about this rela- very interesting host/parasite relationship. Four tionship is the relation of C. turbinatum with only species of the suborder Amblycera were recorded birds of Accipitriformes and absence of other birds before from this bird (Price et al. 2003). The absence of prey of order . This fact supports of from osprey is very questionable. the molecular investigation and separation of the Members of this suborder are common through new order Accipitriformes. many other species of Accipitriformes and these birds are hosts for many ischnoceran species in The most important question now is why the several genera including Aegypoecus spp., bird ancestor of Accipitriformes radiated and Craspedorrhynchus spp., Degeeriella spp. and separated into many different species while the Falcolipeurus spp. (Kellogg 1914; Bedford 1931; chewing louse Colpocephalum turbinatum did not? Clay 1958). As the lice of the suborder Ischnocera The answer to this question lies in the nature of are sluggish and show a high degree of host speci- this species of louse itself. Colpocephalum ficity, we expect that scientists will discover very turbinatum is a cosmopolitan species found every- characteristic new species of ischnoceran chewing where and parasitises a huge number of bird lice from osprey in the future. species through three bird orders Accipitriformes, From the faunistic point of view, Kurodaia Columbiformes and Strigiformes (Adly et al. 2019). haliaeeti (Denny, 1842) of family Menoponidae is Also, this species of louse ventures outside its host the only specific louse of osprey while the other and it was recorded through their host habitat be- three chewing lice species which were recorded fore (Clay 1948). Combining these facts indicates on it before showed a wider range of host rela- that Colpocephalum turbinatum could support one tions. Colpocephalum napiforme Rudow, 1869 and gene pool that prevents its members from isola- Laemobothrion maximum are known from several tion and consequently speciation. The migration species of raptors including many of aquatic birds of host birds also supports the stability of this gene such as African Fish Eagle and Grey-headed fish pool over a long period of time. eagle, while Colpocephalum turbinatum occurs Finally, the information concerning host/para- mainly on Columbiformes and transfer to their site interaction and distribution is very valuable to hosts on order Accipitriformes and Strigiformes study birds’ phylogeny and evolution (Hafner & (Clay 1976). The occurrence of Colpocephalum Nadler 1988). The record of C. turbinatum from turbinatum on marine birds of prey such as osprey osprey could reveal the nature of the ancestor of needs more analysis of osprey evolution to get a this bird that was a terrestrial hunter. Also, it helps complete understanding of this relation. the ornithologists to confirm their phylogenetic Although there are good fossil records of many analysis and improve their wariness about the aquatic ancestors of modern osprey (Mayr 2006), evolution and ecology of these host birds. the new molecular phylogenetic analysis indi- cated that lineage of osprey evolution is separated ACKNOWLEDGEMENTS from other and occurs as paraphyletic This work forms part of a Ph.D. study of the first to it (Fig. 2). The whole cluster shares a common author on the diversity of chewing lice associated ancestor,and scientists think that this ancestor was with the bird fauna of Saudi Arabia, supported by a completely terrestrial bird of prey (Lerner & a graduate student grant from King Abdulaziz Mindell 2005). The other Falconiformes occurs as City for Science and Technology (No. 0003-13- out group of this cluster so ornithologists induced T-A). We are gratefully for kind support and help new order Accipitriformes from this part of old given to this study by the King Saud University, Falconiformes (Christidis & Boles 2008). Deanship of Scientific Research and College of Although the complex distribution of the genus Food and Agriculture Science Research Center. Colpocephalum among bird groups, testing the Our appreciation also goes to HH Prince Bander distribution pattern of Colpocephalum turbinatum Bin Saud Bin Mohammad, the president of Saudi among birds of prey indicated that the restriction Wildlife Authority, for his sponsorship of the study of this distribution is to Acciptridae and its closely of ectoparasites of wild birds in the kingdom. Also, related osprey. This could prove that the ancestor we would like to thank the Saudi Wildlife Com- of this louse was transferred from of Columbi- mittee for supporting this study in the field. Nasser et al.: An analysis of osprey/chewing lice interaction with a new record for Saudi Arabia 183

Fig. 2. Phylogeny of Acciptridae and some other Falconiformes, including osprey (yellow highlighting), based on mitochondrial Cyt-b, ND2 and nuclear b-fibrinogen intron 7 sequences. From this tree we can recognise osprey as being paraphyletic to the Acciptridae, but it is very close to the family; this led to new classification of birds of prey by extracting this group of raptors from the Falconiformes and erecting a new order Accipitriformes that includes osprey. Colpocephalum turbinatum chewing louse, which is common among Accipitriformes, might have been transfered to the terrestrial ancestors of these groups millions of years ago from their terrestrial prey, namely the ancestors of pigeons (red dot). (Adapted from Lerner & Mindell 2005.) 184 African Entomology Vol. 27, No. 1, 2019

§ ORCID iDs M. Ansari: orcid.org/0000-0002-8718-3078 M. Nasser: orcid.org/0000-0001-8627-7833 E. Adly: orcid.org/0000-0002-3510-8105

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