Ticks collected from birds in the northern provinces of South Africa , 2004 – 2006

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.


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 associated tick-borne pathogens across geographical barriers 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 is especially birds that may introduce certain tick species with their associated tick-borne pathogens to new areas, once climate change or human impact has made these habitable for them.Birds readily cross fences between wildlife reserves and pastures used by domestic livestock, and may thus transfer both ticks and tick-borne pathogens from their potential wildlife reservoirs to domestic animals.Moreover acaricide resistance is a considerable 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 objective in the present study was to provide additional 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 ornithologists provide a valuable opportunity for the collection of ectoparasites from the birds they have captured.This study was carried out in collaboration with the members of the Pretoria Bird Ringing Club during their activities at various localities in the provinces of Gauteng, Limpopo, Mpumalanga and North West, South Africa (Table 1).The birds were caught in mist nets and examined for ticks using headmounted magnifying glasses.The examination concentrated 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 increased the handling time of the birds by about one minute.Ticks and other ectoparasites were collected by means of forceps and placed in separate vials containing 70 % ethanol, together with a label recording date, ring number, locality and bird species.We have followed the nomenclature proposed by Hockey, Dean & Ryan (2005) for the birds we examined, and their migration and feeding habits are summarized in Appendix 1.Approximately 3 000 birds were examined, but unfortunately the documents 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 comprised 48 larvae, 124 nymphs and six adults belonging 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

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 species 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-  (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 transportation 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-established as a valid species (Apanaskevich & Horak 2006).
Adult A. marmoreum, the second most common species recovered in this study, feed nearly exclusively 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).Amblyomma 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 distribution is confined to south-eastern Africa (Walker et al. 2003), and it is the tick species of which the immature stages have most often been recorded biting 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 distribution range the immature stages of A. hebraeum are the most common ticks found on Helmeted Guineafowl (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 passerines and other small birds in our study, even though it was conducted within the distribution range of the tick.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 domestic ungulates and dogs, transmit any pathogens (Walker et al. 2003).

Rhipicephalus (Boophilus) decoloratus transmits
Babesia bigemina, A. marginale and Borrelia theileri, the first two of which are causes of cattle diseases 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 Rhipicephalus sanguineus complex, and could be a vector of Rickettsiae of the Spotted fever group (Matsumoto, Ogawa, Brouqui, Raoult & Parola 2005).Large carnivores 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 nestdwelling) (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 development on birds (Cumming 1998;Walker et al. 2003).Our results agree with those of previous surveys 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-moreum, while other ticks seem to be rare or occasional 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 Cinnamon-breasted Bunting are nomadic when not breeding (Sinclair, Hockey & Tarboton 2002), and may therefore be important in long distance dispersal 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 conditions, and may thereby also transport ticks.

CONCLUSION
Birds that feed on the ground are predisposed to tick infestation, but there are also considerable differences 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 infest 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 veterinary importance seem to use small birds as maintenance hosts.

TABLE 2
Ticks collected from 83 infested birds in the northern provinces of South Africa (immature stages when not otherwise indicated) 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 specimens 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 Doublebanded Sandgrouse.A single Rhipicephalus (Boophilus) 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.