Hasle_167-175.indd INTRODUCTION Ticks are important vectors of pathogens affecting humans and livestock, and may themselves cause anaemia, hide damage, and wounds resulting in secondary bacterial infections (Fletcher 2007). An understanding of their dispersal mechanisms is cru- cial towards their effective control. Ticks have very limited locomotor ability and rely on their hosts for dispersal. Migratory birds can serve as hosts for several tick species (Hoogstraal, Kaiser, Traylor, Gaber & Guindy 1961; Hoogstraal, Kaiser, Traylor, Guindy & Gaber 1963; Hoogstraal 1972; Mehl, Michaelsen & Lid 1984; Olsén, Jaenson & Bergström 1995), and may transport these with their associat- ed tick-borne pathogens across geographical barri- ers such as deserts and oceans. In addition, larger, ground-living birds, such as Francolin, Spurfowl and Guineafowl, are important hosts for the immature stages of certain tick species, and are often heavily infested (Horak & Williams 1986; Horak, Fourie, Novellie & Williams 1991a; Horak, Spickett, Braack & Williams 1991b; Horak & Boomker 1998; Uys & Horak 2005). Although passerines and other small birds usually harbour only small numbers of ticks, they often occur in flocks, and thus, because of their large numbers and extraordinary mobility, have the potential of significantly contributing to pathogen dispersal as well as tick gene flow within a region. It 167 Onderstepoort Journal of Veterinary Research, 76:167–175 (2009) Ticks collected from birds in the northern provinces of South Africa, 2004–2006 G. HASLE1*, I.G. HORAK2, G. GRIEVE3, H.P. LEINAAS4 and F. CLARKE5 ABSTRACT HASLE, G., HORAK, I.G., GRIEVE, G., LEINAAS, H.P. & CLARKE, F. 2009. Ticks collected from birds in the northern provinces of South Africa, 2004–2006. Onderstepoort Journal of Veterinary Research, 76:167–175 Approximately 3 000 birds, mainly passerines, caught in mist nets in the northern provinces of South Africa, were examined for ticks. A total of 178 ticks, belonging to 14 species, were recovered from 83 birds of 43 different species. Hyalomma rufipes was the most numerous tick, with 26 larvae and 109 nymphs collected, followed by Amblyomma marmoreum, with 13 larvae and two nymphs. Despite the study being conducted within the distribution range of Amblyomma hebraeum, it was not seen on any passerines, whereas three larger species were infested. The potential for small birds to spread ticks with their associated tick-borne pathogens is discussed. Keywords: Amblyomma marmoreum, birds, Hyalomma rufipes, migration, northern South Africa, passerines, ticks * Author to whom correspondence is to be directed. E-mail: hasle@reiseklinikken.no 1 Oslo Travel Clinic, St Olavs plass 3, NO-0165 Oslo, Norway 2 Department of Veterinary Tropical Diseases, Faculty of Vet er- inary Science, University of Pretoria, Private Bag X04, Onder- stepoort, 0110 South Africa, and Department of Zoology and Entomology, University of the Free State, P.O. Box 339, Bloemfontein, 9300 South Africa 3 Birdlife Northern Gauteng Ringing Group, 344 Delphinus Street, Waterkloof Ridge, Pretoria, 0181 South Africa 4 Department of Biology, University of Oslo, P.O. Box 1066 Blindern, NO-0316 Oslo, Norway 5 Department of Biology, University of Limpopo (Medunsa Campus), P.O. Box 139, Medunsa, 0204 South Africa Accepted for publication 22 August 2008—Editor 168 Ticks collected from birds in northern provinces of South Africa, 2004–2006 is especially birds that may introduce certain tick species with their associated tick-borne pathogens to new areas, once climate change or human im- pact has made these habitable for them. Birds read- ily cross fences between wildlife reserves and pas- tures used by domestic livestock, and may thus transfer both ticks and tick-borne pathogens from their potential wildlife reservoirs to domestic ani- mals. Moreover acaricide resistance is a consider- able problem in some regions of Africa (Fletcher 2007), and it is not entirely unlikely that birds play some role in the spread of acaricide-resistant strains of ticks. Few data sets exist on the ticks that infest small birds in sub-Saharan Africa. However, Horak et al. (1991a) have recorded the immature stages of two tick species on four species of small birds in the Eastern Cape Province, South Africa and in a more recent study Van Niekerk, Fourie & Horak (2006) recorded ticks on 39 species of birds in the Free State Province, South Africa. Amongst the latter there were 28 different passerine species. Our ob- jective in the present study was to provide addition- al data on ticks and the species of birds that they might infest, as well as on the bird species that could be important in spreading ticks. MATERIALS AND METHODS The bird-ringing excursions of amateur ornitholo- gists provide a valuable opportunity for the collec- tion of ectoparasites from the birds they have cap- tured. This study was carried out in collaboration with the members of the Pretoria Bird Ringing Club during their activities at various localities in the prov- inces of Gauteng, Limpopo, Mpumalanga and North West, South Africa (Table 1). The birds were caught in mist nets and examined for ticks using head- mounted magnifying glasses. The examination con- centrated on the head of the birds, especially the eyelids, around the beak and in the ears, where the vast majority of ticks usually occur on passerines (Mehl et al. 1984; Smith 2001). The bare skin under the wings, the brood patch and the region around the cloaca were also frequently examined, but these sites yielded no ticks. The examination for ticks in- creased the handling time of the birds by about one minute. Ticks and other ectoparasites were collect- ed by means of forceps and placed in separate vials containing 70 % ethanol, together with a label re- cording date, ring number, locality and bird species. We have followed the nomenclature proposed by Hockey, Dean & Ryan (2005) for the birds we exam- ined, and their migration and feeding habits are summarized in Appendix 1. Approximately 3 000 birds were examined, but unfortunately the docu- ments recording the exact number were lost. RESULTS The method of trapping birds in mist nets is suitable only for small birds, and most of the birds caught were passerines. Out of a total of approximately 3 000 birds examined, belonging to 43 species, we recovered 178 ticks from 83 of them. The ticks com- prised 48 larvae, 124 nymphs and six adults be- longing to 14 species (Table 2). Among these were one Argas, one Hyalomma and an Ixodes species that we could not identify. The birds that harboured most ticks were Olive Thrush and Cape Robin-Chat. The most numerous tick collected was Hyalomma rufipes, comprising 26 larvae and 109 nymphs. The second most common species was Amblyomma TABLE 1 Localities at which ticks were collected from birds in the northern provinces of South Africa No. Locality Coordinates 1 2 3 4 5 6 7 8 9 10 11 12 13 Buffelsdrift, Pretoria Colbyn, Pretoria Groenkloof, Pretoria Jaleoda Ntsinini, Sagewood cottage Nylsvley Olifantskop Rietvlei Samrand, Midrand Suikerbosrand NR, Kareekloof gate Sunbird Hill, Kameelfontein Wakkerstroom Retirement forest, Wakkerstroom 25°35’ S 25°44’ S 25°47’ S 25°57’ S 25°36’ S 24°39’ S 23°58’ S 25°55’ S 25°55’ S 26°31’ S 25°38’ S 27°21’ S 27°18’ S 28°20’ E 28°15’ E 28°12’ E 28°35’ E 30°23’ E 28°42’ E 27°28’ E 28°18’ E 28°08’ E 28°10’ E 28°24’ E 30°06’ E 30°19’ E 169 G. HASLE et al. TABLE 2 Ticks collected from 83 infested birds in the northern provinces of South Africa (immature stages when not otherwise indi- cated) Tick and bird species Bird species names No. Localities* Birds Ticks Argas species Cardinal Woodpecker Dendropicos fuscescens 1 1 7 Amblyomma hebraeum Swainson’s Spurfowl Southern Yellow-billed Hornbill Double-banded Sandgrouse Pternistis swainsonii Tockus leucomelas Pterocles bicinctus 1 2 1 1 2 1 1 7 7 Amblyomma marmoreum Double-banded Sandgrouse Cattle Egret Brown-crowned Tchagra Red-headed Weaver Red-billed Quelea Cinnamon-breasted Bunting Pterocles bicinctus Bubulcus ibis Tchagra australis Anaplectes melanotis Quelea quelea Emberiza tahapisi 1 1 2 1 1 6 2 2 2 1 1 7 7 1 7, U 7 7 7 Haemaphysalis elliptica Rattling Cisticola Levailant’s Cisticola Long-tailed Widowbird Cisticola chiniana Cisticola tinniens Euplectes progne 1 2 1 1 3 1 1 3, 12 8 Haemaphysalis hoodi Striped Pipit1 Anthus lineiventris 1 1 5 Hyalomma glabrum Red-billed Quelea Cinnamon-breasted Bunting Quelea quelea Emberiza tahapisi 1 1 1 1 7 7 Hyalomma rufipes Striped Kingfisher Red-faced Mousebird Laughing Dove Brown-crowned Tchagra Southern Boubou Crimson-breasted Shrike Common Fiscal Magpie Shrike Southern Black Tit Ashy Tit Dark-capped Bulbul Black-chested Prinia Sabota Lark Kurrichane Thrush Olive Thrush Marico Flycatcher Southern Black Flycatcher Cape Robin-chat Wattled Starling Halcyon chelicuti Urocolius indicus Streptopelia senegalensis Tchagra australis Laniarius ferrugineus Laniarius atrococcineus Lanius collaris Corvinella melanoleuca Parus niger Parus cinerascens Pycnonotus tricolor Prinia flavicans Calendulauda sabota Turdus libonyanus Turdus olivaceus Bradornis mariquensis Melaenornis pammelaina Cossypha caffra Creatophora cinerea 1 1 1 3 2 1 1 1 2 3 2 1 1 2 2 2 2 7 1 3 1 1 13 2 1 1 1 4 7 2 1 2 2 26 5 3 25 1 11 7 7 1, 7, 10 1, 5 7 1 1 7 7 3 10 7 3, 5 10 7 6, U 1, 10, U 10 170 Ticks collected from birds in northern provinces of South Africa, 2004–2006 marmoreum, with 13 larvae and two nymphs. Five specimens of Haemaphysa lis elliptica were also re- covered, one of these from a Rattling Cisticola and three from Levailant’s Cisticola. No other ticks were found on Cisticola. Between one and four speci- mens of the remaining tick species were collected. Amblyomma hebraeum was not found on any of the smaller birds, but was present on Swainson’s Spur- fowl, Southern Yellow-billed Hornbill and Double- banded Sandgrouse. A single Rhipicephalus (Bo- ophilus) decoloratus larva was collected from a Three-banded Plover. The only adult ticks recovered were Ixodes spinae, Ixodes theilerae and Rhipicephalus turanicus. The sole Argas specimen was a larva collected from a Cardinal Woodpecker. Tick and bird species Bird species names No. Localities* Birds Ticks Lesser Masked-weaver Southern Masked-weaver Red-billed Quelea Blue Waxbill Pin-tailed Whydah Cape Longclaw Ploceus intermedius Ploceus velatus Quelea quelea Uraeginthus angolensis Vidua macroura Macronyx capensis 1 4 3 1 1 1 1 19 3 1 1 9 7 7, 11 4, 7 1 7 10 Hyalomma species Cinnamon-breasted Bunting Emberiza tahapisi 1 1 7 Ixodes pilosus group Levaillant’s Cisticola Yellow-crowned Bishop Cisticola tinniens Euplectes afer 1 1 1 1 2 4 Ixodes species Bar-throated Apalis Cape Robin-chat Blue Waxbill Apalis thoracica Cossypha caffra Uraeginthus angolensis 2 1 1 2 1 1 5 5 11 Ixodes spinae Southern Red Bishop1, 2 Euplectes orix 1 1 9 Ixodes theilerae Cape Batis2 Olive Thrush3 Cape Weaver1, 2 Batis capensis Turdus olivaceus Ploceus capensis 1 1 1 1 1 1 13 10 10 Rhipicephalus (Boophilus) decoloratus Three-banded Plover Charadrius tricollaris 1 1 1 Rhipicephalus turanicus Marsh Owl4 Asio capensis 1 3 6 * Numbers in this column refer to localities in Table 1 1 Tick species identity uncertain 2 Adult tick: female 3 The same bird also carried two nymphs of H. rufipes 4 Adult ticks: one female, two males U = unknown 171 G. HASLE et al. DISCUSSION Most ticks were recovered from birds that feed mainly on the ground, in particular members of the family Turdidae. This agrees with the results of an earlier study conducted elsewhere (Olsén et al. 1995). Only a few of the mainly arboreal bird spe- cies that we examined harboured ticks, e.g. the Dark-capped Bulbul and the Lesser Masked- Weaver (see Appendix 1). Because these species are often caught in nets, it is sometimes possible to detect even a low rate of tick infestation on them. After an exhaustive study of numerous specimens of all stages of development of the subspecies of the Hyalomma marginatum group, Apanaskevich & Horak (2008) concluded that these ticks should be treated as independent species, namely H. margi- APPENDIX 1 Species characteristics of the tick-infested birds in the study (Hockey et al. 2005) Bird species Migration habits Feeding habitats Swainson’s Spurfowl* Resident and sedentary On ground Cardinal Woodpecker* Resident and sedentary In trees Southern Yellow-billed Hornbill* Resident and sedentary. Rarely forms small flocks during dry season and drought Mainly on the ground Striped Kingfisher* Resident, with some local movement Mainly on ground in arid areas Red-faced Mousebird* Generally resident, locally nomadic in response to phenology of fruiting trees. Altitudinal migrant Flowers and fruits Marsh Owl* Resident where habitat is stable, otherwise nomadic Lives on ground, eats rodents Laughing Dove* Largely sedentary with some local nomadic movements Open ground Double-banded Sandgrouse* Sedentary. May move in search of water On ground Three-banded Plover* Sedentary. Partial intra-African migrant in response to seasonal rainfall On open shores Cattle Egret* Moves over large distances On ground Brown-crowned Tchagra Resident and sedentary On ground Southern Boubou Resident and sedentary On ground Crimson-breasted Shrike Resident and sedentary, but may move locally to riverine woodland during non-breeding season On ground and in trees Cape Batis Resident. Altitudinal migration In trees Common Fiscal Mostly resident and sedentary, possibly nomadic Small prey usually eaten on ground Magpie Shrike Resident and generally sedentary, but may move locally in response to drought and fires Mostly on ground Southern Black Tit Resident Mainly in trees, eats earthworms after rain Ashy Tit Resident and locally nomadic In bushes, less frequently on ground Dark-capped Bulbul Sedentary. Some local dispersal linked to food availability In trees, occasionally on ground Rattling Cisticola Resident Low in grass or bushes, or on ground Levailant’s Cisticola Mostly resident, may undertake local movements Low down in vegetation 172 Ticks collected from birds in northern provinces of South Africa, 2004–2006 natum, H. rufipes, H. isaaci and H. turanicum, and we have followed their recommendation. Hyalomma rufipes was the most prevalent tick species on small birds in our survey as well as in other studies (Hoog- straal et al. 1961; Van Niekerk et al. 2006). Adult H. rufipes feed on large ungulates (Norval 1982), and the immature stages feed on birds (Horak et al. 1991b; Uys & Horak 2005; Van Niekerk et al. 2006), and hares (Horak & Fourie 1991). It is patchily dis- tributed in Africa, Europe and Western and Central Asia (Walker, Bouattour, Camicas, Estrada-Peña, Horak, Latif, Pegram & Preston 2003), and is the most important vector of C rimean-Congo haemor- rhagic fever (CCHF) virus to humans in South Africa Bird species Migration habits Feeding habitats Black-chested Prinia Resident. Probably locally nomadic In bushes, less frequently on ground Bar-throated Apalis Resident and sedentary. Some winter movements to lower altitudes Partly on ground Sabota Lark Resident and sedentary, locally nomadic in drier part of range On ground Kurrichane Thrush Mainly resident. Some altitudinal migration On ground Olive Thrush Mostly resident, altitudinal migrant, and in response to drought Mostly on ground Marico Flycatcher Resident Mostly on ground Southern Black Flycatcher Resident Partly on ground Cape Robin-Chat Altitudinal migrant Spends much time on ground Wattled Starling Nomadic Mostly on ground Lesser Masked-Weaver Resident, sedentary and local nomad In tree canopies Cape Weaver Mostly resident and sedentary, with some local movements. 5% move >100km On ground Southern Masked-Weaver Resident, sedentary and partial migrant On ground, grass stems and trees Red-headed Weaver In Botswana, moves out of deciduous woodland in dry season; in Zimbabwe, range contracts in non-breed- ing season Mainly in trees, bushes and creepers Red-billed Quelea Large scale movements throughout range On ground Yellow-crowned Bishop Resident and locally nomadic. Migratory in West Africa On ground or directly from plants Southern Red Bishop Resident and sedentary, some local movement in non-breeding season Both on ground and perched in vegetation Long-tailed Widowbird Resident and sedentary, local movement in non- breeding season. Largely on ground Blue Waxbill Mostly resident. May move nomadically in winter On ground and in vegetation Pin-tailed Whydah Resident and sedentary. Nomadic in non-breeding season Eat seeds on ground Cape Longclaw Resident. Form groups on burnt ground in winter On ground Striped Pipit Resident and sedentary, possibly with some local movement On ground Cinnamon-breasted Bunting Resident, but migrant from Nov-Dec to April-May On ground * = non-passerine species 173 G. HASLE et al. (Horak, Swanepoel & Gummow 2002). In Africa it may also transmit Anaplasma marginale, Rickettsia conorii and Babesia occultans (Walker et al. 2003). Unlike other tick species, of which the immature stages tend to infest mainly larger birds, H. rufipes is found on passerines (Cumming 1998) as well as on larger species such as Crested Francolin and Helmeted Guineafowl (Horak et al. 1991b; Uys and Horak 2005). It is a two-host tick, which, like its close relative H. marginatum, probably remains attached to the host for 12 to 26 days from the start of feeding of the larva to detachment of the engorged nymph (Hueli 1979). This prolonged period of attachment plays an important role in the long-distance trans- portation of ticks with their associated tick-borne pathogens. The immature stages of Hyalomma glabrum, which we collected from two birds, infest hares and birds (Apanaskevich & Horak 2006). This tick, which was previously thought to be Hyalomma turanicum, a known vector of CCHF, has recently been re-estab- lished as a valid species (Apanaskevich & Horak 2006). Adult A. marmoreum, the second most common species recovered in this study, feed nearly exclu- sively on tortoises (Horak, McKay, Heyne & Spickett 2006). Its immature stages feed on a wide range of hosts, including tortoises and birds (Horak et al. 2006; Van Niekerk et al. 2006). This tick may play a role in the transmission of Ehrlichia ruminantium to domestic ruminants (Norval & Horak 2004). Ambly- omma hebraeum, which in the present study was collected from three of the larger bird species, is the major vector of E. ruminatium in South Africa (Norval & Horak 2004). It also transmits Theileria mutans to cattle, and Rickettsia africae to humans. Its distribu- tion is confined to south-eastern Africa (Walker et al. 2003), and it is the tick species of which the im- mature stages have most often been recorded bit- ing humans in South Africa (Horak, Fourie, Heyne, Walker & Needham 2002). The adults prefer large ungulates, while the immature stages parasitize large and small ungulates as well as large ground living birds (Walker et al. 2003). Within its distribu- tion range the immature stages of A. hebraeum are the most common ticks found on Helmeted Guinea- fowl (Horak & Williams 1986; Horak et al. 1991b), and they are also common on Crested Francolin (Uys & Horak 2005). Despite large numbers of birds being examined in earlier studies, adult ticks were not encountered on them (Horak & Williams 1986; Horak et al. 1991b; Uys & Horak 2005). Amblyomma hebraeum is apparently not spread by small birds, as no ticks of this species were collected from pas- serines and other small birds in our study, even though it was conducted within the distribution range of the tick. Haemaphysalis elliptica (formerly H. leachi) (Apa- nas kevich, Horak & Camicas 2007), the third most common tick collected (Table 2), is a major vector of Babesia canis to dogs, and can transmit R. conorii to humans. It is a parasite of large domestic and wild carnivores, and is widespread in southern Africa (Apanaskevich et al. 2007). True H. leachi is found in the Nile delta and north-east Africa (Walker et al. 2003). The immature stages of H. elliptica are not common parasites of birds. Van Niekerk et al. (2006) recovered a single nymph from birds in Free State Province, while Horak et al. (1991b) collected only three larvae and two nymphs from 118 Helmeted Guineafowl, as opposed to 23 778 A. hebraeum and 2 387 A. marmoreum larvae and nymphs from the same birds in a habitat in which all three tick spe- cies were abundant. It is not known whether Haemaphysalis hoodi and I. theilerae, which parasitize birds, and I. spinae which infests birds, hyraxes and rodents (Cumming 1998), or Ixodes pilosus, which parasitizes wild and do- mestic ungulates and dogs, transmit any pathogens (Walker et al. 2003). Rhipicephalus (Boophilus) decoloratus transmits Babesia bigemina, A. marginale and Borrelia thei- leri, the first two of which are causes of cattle dis- eases of immense veterinary importance in South Africa. This is a one-host tick (Walker et al. 2003), and should be considered an accidental parasite of birds, on which it is unlikely to complete its life cycle. Rhipicephalus turanicus belongs to the Rhipiceph- alus sanguineus complex, and could be a vector of Rickettsiae of the Spotted fever group (Matsumoto, Ogawa, Brouqui, Raoult & Parola 2005). Large car- nivores and large ground-living birds are hosts of the adults of this species (Walker, Keirans & Horak 2000), which we collected from a Marsh Owl. Argasids are typically endophilic (burrow or nest- dwelling) (Hillyard 1996), and this may explain why an Argas species was found on a woodpecker. We found no tick species in this study that had not previously been recorded in the same stage of de- velopment on birds (Cumming 1998; Walker et al. 2003). Our results agree with those of previous sur- veys in that the immature stages of H. rufipes are the most common tick species found on passerines and other small land birds, followed by A. mar- 174 Ticks collected from birds in northern provinces of South Africa, 2004–2006 moreum, while other ticks seem to be rare or occa- sional parasites (Horak et al. 1991a; Van Niekerk et al. 2006). Strangely, none of the ticks recovered in this study were from migratory birds that breed in temperate regions, and which travel large distances every day during the migration seasons. Few South African birds migrate regularly. Red-billed Quelea and Cin- namon-breasted Bunting are nomadic when not breeding (Sinclair, Hockey & Tarboton 2002), and may therefore be important in long distance disper- sal of ticks. Sedentary birds like Cape Robin-Chat may move within their distributional range during winter, or to KwaZulu Natal, where they are seen as winter visitors (Sinclair et al. 2002). Some species are altitudinal migrants, e.g. Bar-Throated Apalis and Cape Robin-Chat (Hockey et al. 2005). Almost all bird species move about in search of food and water, particularly during harsh environmental con- ditions, and may thereby also transport ticks. CONCLUSION Birds that feed on the ground are predisposed to tick infestation, but there are also considerable dif- ferences among tick species in their predisposition and ability to infest birds. The immature stages of H. rufipes and A. marmoreum infest small birds, like passerines, but they may also infest larger birds. Conversely the immature instars of A. hebraeum in- fest larger birds, but apparently not passerines. The overall widespread distribution of H. rufipes may in part be ascribed to its tendency to infest passerines. Ticks (including acaricide-resistant ticks) with their associated tick-borne pathogens may be dispersed over large distances via bird migration. Smaller birds, through their huge numbers, may play a role as hosts for ticks, but no ticks of medical or veteri- nary importance seem to use small birds as mainte- nance hosts. ACKNOWLEDGEMENTS This survey is a part of an ectoparasite study ap- proved by the ethical and scientific review commit- tee of the University of Limpopo (Medunsa Campus). G. Hasle’s participation in the study was supported by a travel grant from Abbott, Norway. REFERENCES APANASKEVICH, D.A., & HORAK, I.G. 2006. The genus Hy a- lomma Koch, 1844. I. 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