Parasites of domestic and wild animals in South Africa. XLVII. Ticks of tortoises and other reptiles.

INTRODUCTION Reptiles in southern Africa are hosts of several spe- cies of ixodid ticks (Theiler 1962). The majority of these ticks belong to the genus Amblyomma, of which nine species, including three species that be- longed to the former genus Aponomma (now Ambly- omma), occur in South Africa (Walker 1991). Theiler (1943, 1945a, b) has published illustrations of Ambly- omma sylvaticum and of the ornate and inornate Aponommas. The latter ticks have recently been placed in the genus Amblyomma and are now des- ignated Amblyomma exornatum, Amblyomma latum and Amblyomma transversale (Klompen, Dobson & Barker 2002). Theiler & Salisbury (1959) have illus- 215 Onderstepoort Journal of Veterinary Research, 73:215–227 (2006) Parasites of domestic and wild animals in South Africa. XLVII. Ticks of tortoises and other reptiles I.G. HORAK1, I.J. MCKAY2*, B.T. HENEN3, HELOISE HEYNE2, MARGARETHA D. HOFMEYR3 and A.L. DE VILLIERS4 ABSTRACT HORAK, I.G., MCKAY, I.J., HENEN, B.T., HEYNE, HELOISE, HOFMEYR, MARGARETHA D. & DE VIL LIERS, A.L. 2006. Parasites of domestic and wild animals in South Africa. XLVII. Ticks of tortoises and other reptiles. Onderstepoort Journal of Veterinary Research, 73:215–227 A total of 586 reptiles, belonging to 35 species and five subspecies, were examined in surveys aimed at determining the species spectrum and geographic distribution of ticks that infest them. Of these rep- tiles 509 were tortoises, 28 monitor or other lizards, and 49 snakes. Nine ixodid tick species, of which seven belonged to the genus Amblyomma, and one argasid tick, Ornithodoros compactus were re- covered. Seven of the ten tick species are parasites of reptiles. Amongst these seven species Am bly- omma marmoreum was most prevalent and numerous on leopard tortoises, Geochelone pardalis; Amblyomma nuttalli was present only on Bell’s hinged tortoises, Kinixys belliana; and most Amblyomma sylvaticum were collected from angulate tortoises, Chersina angulata. Amblyomma exornatum (for- merly Aponomma exornatum) was only recovered from monitor lizards, Varanus spp.; most Ambly- omma latum (formerly Aponomma latum) were from snakes; and a single nymph of Amblyomma trans versale (formerly Aponomma transversale) was collected from a southern African python, Python natalensis. All 30 Namaqualand speckled padloper tortoises, Homopus signatus signatus, examined were infested with O. compactus. The seasonal occurrence of A. sylvaticum and the geographic distribution of this tick and of A. mar- moreum, A. nuttalli, A. exornatum, A. latum and O. compactus are illustrated. Keywords: Amblyomma spp., argasid tick, geographic distribution, ixodid ticks, Ornithodoros com- pactus, reptiles, seasonality, snakes, tortoises, varanid lizards 1 Department of Veterinary Tropical Diseases, Faculty of Vet- erinary Science, University of Pretoria, Onderstepoort, 0110 South Africa, and Division of Parasitology, ARC-Onderstepoort Veterinary Institute, Onderstepoort, 0110 South Africa 2 Division of Parasitology, ARC-Onderstepoort Veterinary Insti- tute, Onderstepoort, 0110 South Africa. * Dr McKay’s present address is: School of Geosciences, University of Witwaters rand, Private Bag X3, Wits, 2050 South Africa 3 Chelonian Biodiversity and Conservation - Southern Africa, De part ment of Biodiversity and Conservation Biology, Univer- sity of the Western Cape, Private Bag X17, Bellville, 7535 South Africa 4 Scientific Services, Western Cape Nature Conservation Board, Private Bag X5014, Stellenbosch, 7599 South Africa Accepted for publication 12 April 2006—Editor

216 Parasites of domestic and wild animals in South Africa. XLVII trated ticks of ‘the Amblyomma marmoreum group’, and colour illustrations of Amblyomma hebraeum and A. marmoreum have been published by Walker & Olwage (1987). A single argasid species, Ornitho- doros compactus infests tortoises in southern Africa, and has been illustrated by Walton (1962). Theiler (1962) has listed the reptile species and the localities in sub-Saharan Africa from which ticks of the genera Amblyomma and Aponomma (now Am- bly omma) have been collected. Norval (1983, 1985) has recorded the hosts and mapped the localities at which Amblyomma nuttalli, A. marmoreum, A. exor- natum, A. latum and A. transversale have been col- lected in Zimbabwe. Walker & Schulz (1984) have recorded the numbers of A. hebraeum and A. mar- moreum collected from tortoises in the Addo Elephant National Park, Eastern Cape Province, and Dower, Petney & Horak (1988) those collected from leopard tortoises in the Andries Vosloo Kudu Reserve and in the Thomas Baines Nature Reserve, Eastern Cape Province. The seasonality of A. marmoreum on leo- pard tortoises in the National Zoological Gardens, Pre toria, Gauteng Province has been determined by Rechav & Fielden (1995), and the hosts, season- ality and geographic distribution of the latter tick in South Africa have been recorded and illustrated by Horak, McKay, Heyne & Spickett (2006). Walton (1962) has listed the tortoise species from which O. compactus has been collected. With the exception of A. hebraeum and O. compac- tus, the above-mentioned ticks have all been re- corded on reptiles imported into the United States of Amer ica (USA) from Africa (Burridge, Simmons & Allan 2000; Burridge 2001; Burridge & Simmons 2003). This illus trates not only the close association between the ticks and their hosts, but their prolonged periods of attachment, which exceed the length of time from the capture of the reptile in Africa, its trans- location to a foreign country and its legal or illegal importation into that country. Amblyomma marmor- eum has in fact adapted to its new habitat and be- come estab lished at a reptile breeding facility in Flor- ida in the USA (Allan, Simmons & Burridge 1998). According to Walton (1962) the O. compactus re- corded in European zoological gardens, probably arrived there as first stage nymphs on imported tor- toises. The purpose of this paper is to record the species spectrum of ticks that infest tortoises and various other reptiles in South Africa, and to illustrate the seasonality and geographic distributions of those species for which sufficient data exist. MATERIALS AND METHODS The data for this communication are derived from four surveys of ticks parasitizing tortoises and other reptiles. Firstly a study conducted specifically on tortoises, chiefly in the southern provinces of South Africa, be- tween 1975 and 1981, during which all vis ible ticks were collected, but no record was kept of the number of tortoises that were not infested. Sec ondly ticks were collected from tortoises in the West ern and Northern Cape Provinces between 2000 and 2003 as part of a larger investigation on the biol ogy and conservation of these animals. Again no record was kept of the number of tortoises that were not infested. Thirdly from casual collections between 1981 and 2005 from tortoises and other reptiles, and finally studies on 23 leopard tortoises conducted by Dower et al. (1988) and Horak & Boomker (1998) have been included for completeness’ sake. The vast majority of collections were made from free-living reptiles, with a few made from captive animals. With the ex- ception of the study by Dower et al. (1988), in which ticks were recovered after detaching from caged, naturally infested tortoises, ticks were collected man- ually, or by means of pincers, and preserved in 70 % ethyl alcohol for subsequent identification and count- ing. The collections made by Dower et al. (1988) were exhaustive, while the others concentrated on collecting only the visible and hence more easily ac- cessible ticks. The parasite host tables that follow list the total number of tortoises and other reptiles of each species that were infested irrespective of the tick species and the numbers of animals that were infested with particular species. The localities at which ticks were collected were recorded and their geographic coordinates determined and plotted. The results of the collections pertaining to A. mar- moreum have been reported separately (Horak et al. 2006) and, with the exception of the tick-host ta- ble and geographic distribution map, to which new data have been added, they are not repeated here. Large numbers of all stages of development of A. sylvaticum were collected from angulate tortoises during the course of the surveys, and the mean num- bers recovered each month, irrespective of the year, have been used to determine the seasonal occur- rence of this tick on these animals. The maps illus- trating the geographic distributions of the various tick species have been compiled from the coordinates of localities listed by Theiler (1962), as well as from those at which ticks were collected in the surveys reported here.

217 I.G. HORAK et al. We have used Branch (1998) as our primary source of reference for the specific and common names of the tortoise and other reptile species examined. These have been listed in the tables and the scien- tific names will not be repeated in the text. Whenever we have been uncertain of the sub-specific identity of a particular tortoise we have used the geographic distribution maps plotted by Branch (1998), or the habitat preferences of the various sub-species of tent tortoises (Branch 1989), and the field experi- ence of B.T.H. and M.D.H. to arrive at an acceptable solution. When this has not been possible we have used only the specific name of the tortoise. In some cases the animals were identified only as ‘tortoise’ or ‘monitor lizard’ by the collectors and are listed as such in the tables. RESULTS AND DISCUSSION Amblyomma hebraeum The hosts of adult A. hebraeum are large herbivo- rous mammals, whereas the larvae and nymphs can be found on a variety of large and small mammals and on ground-frequenting birds, and the nymphs also on reptiles (Norval 1983; Horak, MacIvor, Pet- ney & De Vos 1987; Dower et al. 1988). Conse quent- ly, despite the fact that A. hebraeum adults were TABLE 1 Ticks collected from various reptile species Tick and host species Number infested with ticks Number infested with spe - cies listed Number of ticks collected Larvae Nymphs Males Females Total Amblyomma hebraeum Leopard tortoise, Geochelone pardalis 31* 19 0 686 20 13 719 Rock monitor, Varanus albigularis albigularis 4* 2 0 33 0 0 33 Amblyomma nuttalli Bell’s hinged tortoise, Kinixys belliana 7 5 0 0 9 0 9 Amblyomma exornatum Rock monitor, V. a. albigularis 7 7 0 112 191 116 419 Water monitor, Varanus niloticus 12 12 0 53 104 75 232 “Monitor”, Varanus spp. 3 3 0 3 17 2 22 Amblyomma transversale Southern African python, Python natalensis 3 1 0 1 0 0 1 Hyalomma truncatum Leopard tortoise, G. pardalis 82 3 0 0 1 3 4 Geometric tortoise, Psammobates geometricus 86 1 0 0 1 0 1 Rhipicephalus gertrudae Geometric tortoise, P. geometricus 86 1 0 0 0 1 1 “Tortoise” 9 1 0 0 2 0 2 * = Number of animals examined within the distribution range of A. hebraeum

218 Parasites of domestic and wild animals in South Africa. XLVII TABLE 2 Amblyomma marmoreum collected from reptiles Host species Number infested with ticks Number infested with A. mar- moreum Number of ticks collected Larvae Nymphs Males Females Total Leopard tortoise, G. pardalis 82 80 336 105 545 217 1 203 Bell’s hinged tortoise, K. belliana 7 2 0 0 5 3 8 Geometric tortoise, P. geometricus 86 68 28 9 64 14 115 Serrated tortoise, Psammobates oculiferus 11 11 0 1 9 4 14 Tent tortoise, Psammobates tentorius tentorius 23 22 0 8 21 11 40 Namaqualand tent tortoise, Psammobates tentorius trimeni 5 1 0 0 1 0 1 Bushmanland tent tortoise, Psammobates tentorius verroxii 11 2 0 0 4 0 4 Tent tortoise, Psammobates tentorius 5 1 1 0 0 0 1 Angulate tortoise, Chersina angulata 138 9 0 6 17 2 25 Common padloper, Homopus areolatus 87 75 68 65 33 21 187 Karoo padloper, Homopus boulengeri 2 2 2 5 0 0 7 Greater padloper, Homopus femoralis 4 4 0 1 4 0 5 Southern speckled padloper, Homopus signatus cafer 8 2 81 0 1 0 82 Namaqualand speckled pad loper, Homopus signatus signatus 30 0 0 0 0 0 0 “Tortoise” 10 8 7 21 23 10 61 Rock monitor, V. a. albigularis 7 3 0 7 1 0 8 “Monitor”, Varanus spp. 3 1 0 2 2 0 4 Southern African python, P. natalensis 3 3 0 11 0 0 11 “Python” 1 1 0 0 0 1 1 Puff adder, Bitis arietans 3 2 0 2 2 0 4 Gaboon adder, Bitis gabonica 1 1 2 0 0 0 2 Common egg eater, Dasypeltis scabra 1 1 0 1 0 0 1 Boomslang, Dispholidus typus 1 1 0 2 0 0 2 Total 529 300 525 246 732 283 1 786

219 I.G. HORAK et al. present on a number of leopard tortoises examined within the tick’s distribution range (Table 1), these infestations must be considered opportune, possibly triggered by A. hebraeum or A. marmoreum males already present on the tortoises. Attached, engorging A. hebraeum males produce pheromones that, with the carbon dioxide exhaled by their hosts, attract con-specific females, other males and nymphs (Nor- val, Yunker & Butler 1987). The life stage spectrum of the ticks attached to the 19 infested leopard tor- toises seems to indicate that male A. marmoreum may also produce pheromones that can be detected by con-specific ticks as well as by A. hebraeum nymphs and adults. Howell, Walker & Nevill (1978) have illustrated the geographic distribution of A. hebraeum within the boundaries of South Africa, and the present records from tortoises all fall within this range. Amblyomma marmoreum This tick, colloquially known as the South African tortoise tick, is probably the species most frequently encountered on tortoises throughout South Africa (Theiler & Salisbury 1959; Horak et al. 2006). It is the largest ixodid tick in South Africa, and engorged females may exceed 25 mm in length. With the ex- ception of angulate and Namaqualand speckled padloper tortoises (the latter the smallest tortoise species in the world), a large percentage of individu- als within each tortoise species were infested (Table 2). It would seem that the larger the species the greater the number of adult ticks it is likely to har- bour, and leopard tortoises, the largest of the South African species, carried most adult ticks. Amongst the latter was a tortoise infested with 63 male and 105 female ticks. The immature stages, particularly larvae, infest not only reptiles, but also a large vari- ety of mammals and birds (Horak et al. 2006). The comparatively small total number of immature ticks collected from the various tortoise species could not sustain the large number of adult ticks collected from these animals. Because complete collections were not always made, large numbers of immature ticks were probably overlooked. Furthermore, the large number of larvae and fewer nymphs that attach to a variety of warm-blooded hosts, both avian and mammalian (Horak et al. 2006), could serve to aug- ment the apparently insufficient numbers of imma- ture ticks collected. Theiler & Salisbury (1959) mapped the distribution of A. marmoreum in South Africa from the geo- graphic coordinates of 49 localities at which collec- tions had been made. Horak et al. (2006) added more than 100 localities to that map and we have now added approximately 70 more sites (Fig. 1). Most collections have been made in the south-western FIG. 1 Geographic distribution of Amblyomma marmoreum in South Africa