Horak_13-25.indd INTRODUCTION The majority of ticks that have been collected from tortoises in South Africa belong to the genus Ambly- omma and of these Amblyomma marmoreum, col- loquially known as the South African tortoise tick, is probably the most prevalent (Theiler & Salisbury 1959). Although records of ticks on tortoises in South Africa date back to the 18th and 19th centuries (Theiler 1943; Walker & Schulz 1984), it was not until Thei- ler & Salisbury (1959) and Norval (1975) published their descriptions of ticks in the “Amblyomma mar- moreum group” and on the ecology of A. marmoreum, respectively, that the taxonomy and biology of the latter tick was comprehensively addressed. In their paper, Theiler & Salisbury (1959) illustrated and de- scribed all stages of development of A. marmoreum 13 Onderstepoort Journal of Veterinary Research, 74:13–25 (2006) Hosts, seasonality and geographic distribution of the South African tortoise tick, Amblyomma marmoreum I.G. HORAK1, I.J. MCKAY2,* HELOISE HEYNE2 and A.M. SPICKETT2 ABSTRACT HORAK, I.G., MCKAY, I.J., HEYNE, HELOISE & SPICKETT, A.M. 2006. Hosts, seasonality and geo- graphic distribution of the South African tortoise tick, Amblyomma marmoreum. Onderstepoort Journal of Veterinary Research, 74:13–25 The tortoise tick Amblyomma marmoreum was collected from large numbers of reptiles and other animals during the course of numerous surveys conducted in South Africa. A total of 1 229 ticks, of which 550 were adults, were recovered from 309 reptiles belonging to 13 species, with leopard tor- toises, Geochelone pardalis being the most heavily infested. The 269 birds sampled harboured 4 901 larvae, 217 nymphs and no adult ticks, and the prevalence of infestation was greatest on hel meted guinea fowls, Numida meleagris. Only two larvae were recovered from 610 rodents, including 31 spring hares, Pedetes capensis, whereas 1 144 other small mammals yielded 1 835 immature ticks, of which 1 655 were collected from 623 scrub hares, Lepus saxatilis. The 213 carnivores examined harboured 2 459 ticks of which none were adult. A single adult tick and 6 684 larvae and 62 nymphs were recovered from 656 large herbivores, and a total of 4 081 immature ticks and three adults were collected from 1 543 domestic animals and 194 humans. Adult male and female A. marmoreum were most numerous on reptiles during January and February, and larvae during March. The largest numbers of larvae were present on domestic cattle and helmeted guineafowls in the Eastern Cape Province during March or April respectively, whereas larvae were most numerous on helmeted guineafowls, scrub hares and the vegetation in north-eastern Mpu malanga Province during May. In both provinces nymphs were most numerous between October and December. Amblyomma marmoreum appears to be most prevalent in the western regions of the Western and Eastern Cape and Free State provinces, and the north-eastern regions of the Northern Cape, KwaZulu- Natal, Mpumulanga and Limpopo provinces. Keywords: Amblyomma marmoreum, birds, carnivores, domestic animals, geographic distribution, large herbivores, reptiles, seasonality, small mammals, vegetation 1 Department of Veterinary Tropical Diseases, Faculty of Vet- erinary Science, University of Pretoria, Onderstepoort, 0110 South Africa, and Department of Zoology and Entomology, University of the Free State, Bloemfontein, 9301 South Africa 2 Department of Parasitology, ARC-Onderstepoort Veterinary Institute, Onderstepoort, 0110 South Africa * Present address: School of Geosciences, University of Wit- watersrand, Private Bag X3, Wits, 2050 South Africa Accepted for publication 22 June 2005—Editor 14 South African tortoise tick, Amblyomma marmoreum and mapped its distribution and supplied a brief host list, while Norval (1975) described its ecology, life cycle and seasonality in the Eastern Cape Province and provided a more comprehensive list of hosts. Some years later Walker & Schulz (1984) recorded the burdens of A. marmoreum on tortoises in the Addo Elephant National Park in the Eastern Cape Province, while Norval (1983) listed its hosts and mapped its distribution in Zimbabwe. Interest in A. marmoreum gained momentum with the unpublished discovery by Bezuidenhout & Oli- vier in 1985 and Bezuidenhout in 1986 (cited by Bezuidenhout 1987, and Oberem & Bezuidenhout 1987) that it could both acquire and transmit Ehrlichia (Cow dria) ruminantium, the causative organism of heart water in domestic and wild ruminants. In addi- tion, Bezuidenhout (1988) demonstrated that the leopard tortoise, a preferred host of all stages of de- velopment of the tick, could be infected with E. (Cowdria) ruminantium and that the tick could ac- quire infection from an infected tortoise. He also demonstrated that two hosts of the immature stag- es, namely hel meted guineafowls and scrub hares could act as sub clinical reservoirs of E. (Cowdria) ruminantium. Walker & Olwage (1987) have published colour il- lustrations of a male and female tick and have mapped the distribution of A. marmoreum in Africa. Horak, MacIvor, Petney & De Vos (1987a) have provided host lists as well as the mean intensity and prevalence of infestation on these hosts, while Dower, Petney & Horak (1988) determined the tick burdens, and the detachment periods and weights of the various life stages of A. marmoreum on natu- rally infested tortoises in the Eastern Cape Province. The pres ence, and occasionally also the season- ality, of the immature stages of A. marmoreum on a large number of host species have been recorded by Horak and his co-workers in several published and unpublished surveys of parasites of domestic and wild animals conducted in South Africa (Horak & Fourie 1986; Horak, Jacot Guillarmod, Moolman & De Vos 1987b; Dower et al. 1988; Fourie & Horak 1990; Horak, Williams & Van Schalkwyk 1991a; Horak, Fourie, Novellie & Williams 1991b; Horak, Spickett, Braack & Williams 1991c; Horak, Knight & Williams 1991d; Horak & Fourie 1991; Horak, Boom- ker, Spickett & De Vos 1992; Horak, Spickett, Braack & Penzhorn 1993; Boomker, Horak & Ram say 1994; Horak & Boomker 1998; Horak 1999; Horak, Braack, Fourie & Walker 2000; Horak, MacIvor & Greeff 2001; Horak, Gallivan, Braack, Boomker & De Vos 2003; Horak & Matthee 2003; Uys & Horak 2005). Fielden, Magano & Rechav (1992) have compared the length of the life cycle of A. marmoreum on tor- toises and on guinea pigs in the laboratory, and Fielden & Rechav (1994) and Rechav & Fielden (1995) have determined its attachment sites and sea sonal abundance on leopard tortoises. Burridge (2001) and Burridge & Simmons (2003) have de- scribed its introduction as well as that of other ticks into the United States of America on imported rep- tiles and Allan, Simmons & Burridge (1998) have re- ported its establishment on a reptile-breeding facil - ity in Florida. Peter, Burridge & Mahan (2000) have demonstrated the competence of A. marmoreum as a potential effective vector of E. (Cow dria) ruminan- tium in that country. The present paper is based on the findings perti- nent to A. marmoreum in the numerous surveys con- ducted in South Africa as well as on a large number of tick collections made from reptiles, particularly tortoises that have not previously been published. Its purpose is to record the presence and the sea- sonality of adult and immature A. marmoreum on tor- toises, and that of its larvae and nymphs on mam- mals and birds as well as of its free-living larvae on vegetation. Furthermore the coordinates of the local- ities at which the abovementioned collections were made have been used to up-date Theiler & Salis- bury’s (1959) map of the tick’s distribution in South Africa. MATERIALS AND METHODS Ticks were collected manually from several live rep- tiles, chiefly tortoises, and preserved in 70 % ethyl alcohol for subsequent identification and counting. Ticks were also collected from domestic and wild animals in various regions of the country, as well as from the vegetation within the Kruger National Park in north-eastern Mpumalanga Province. The tech- niques used to collect ticks in the various surveys have been described by Horak et al. (1987b; 1991c; 1992), Dower et al. (1988) and Spickett, Horak, Van Niekerk & Braack (1992), and are not repeated here. The findings presented pertain only to A. mar- moreum and not to the other ticks collected during the various surveys. The animal species sampled have been divided into six groupings, namely reptiles, birds, small mam- mals, carnivores, large herbivores, and domestic animals and humans, and the numbers of A. mar- moreum collected from each host species within each of the groupings have been summarized in tabular format. The scientific names of the animals 15 I.G. HORAK et al. examined are included in the tables and are not re- peated in the text. The monthly mean adult and immature tick burdens of all tortoises examined over a period 6 years, irre- spective of species and the year in which they were sampled, have been used to construct a pattern of annual seasonality for A. marmoreum. A similar pro- cess has been followed with the immature tick bur- dens of helmeted guineafowls and of cattle exam- ined at monthly intervals over a period of 2 years in the Eastern Cape Province, and of helmeted guinea- fowls and scrub hares examined at monthly inter- vals over periods of 2 and 6 years, respectively in north-eastern Mpumalanga Province. The season- ality of free-living larvae on the vegetation was de- termined from the means of consecutive monthly collections made over a period of 13 years and 8 months in a landscape zone within the southern Kruger National Park. The geographic coordinates of the localities at which the various collections were made have been added to those of Theiler & Salisbury (1959), and have been used to redefine the distribution of A. marmoreum within the borders of South Africa. RESULTS AND DISCUSSION Hosts A total of 309 reptiles belonging to 13 species were examined and with the exception of the Karoo pad- loper, of which only two specimens were sampled, all tortoise species were infested with adult A. mar- moreum (Table 1). The largest numbers of adult and immature ticks were recovered from leopard tor- toises. Comparisons between reptile species are, however, not possible because of differences in the sampling techniques. Most collections were done manually and focused on the more visible and hence detachable ticks, but 14 leopard tortoises were kept in cages over water until all the ticks present on most of them had detached (Dower et al. 1988). The prevalence of infestation on the various spe- cies of reptiles can also not be deduced from the available data as the majority of collections were made from live animals and no records were kept of the number of reptiles on which no ticks were seen. Whereas other animals harbour only the immature stages of A. marmoreum, reptiles, and more particu- larly tortoises, harbour all stages of development. This pattern of host preference dictates that the tick’s life cycle can be completed only in those lo- calities where tortoises and certain other large rep- tile species are present. In the present study the ra- tio of larvae to nymphs to adults on tortoises and other reptiles was 2.7:1.0:3.0, indicating that the number of immature ticks would have been unable to maintain the adult population. However, as most of the collections made from these animals were not design ed to be total recoveries, and focused mainly on the more visible adult ticks, these ratios are not surprising. In a more detailed study on the seasonal occurrence of A. marmoreum, leopard tortoises in a large, fenced enclosure containing natural savanna- type vegetation in the National Zoolog ical Gardens, Pretoria, were examined for ticks at monthly inter- vals (Rechav & Fielden 1995). Over a period of a year the ratio of larvae to nymphs to adults on these animals was 5.7:2.7:1.0, indicating an adequate num- ber of immature ticks to maintain the adult burdens on the tortoises. Five bird species, comprising 269 individuals, were examined for ticks (Table 2). These examinations were thorough as they were conducted on dead birds and hence both the prevalence and intensity of infestation recorded are more reliable than they would have been had they been based on manual collections of ticks from live birds. A large proportion of helmeted guineafowls and francolins were infest- ed and many larvae were collected from these birds. The largest number of ticks recovered from a single guineafowl consisted of 585 larvae and one nymph collected from a bird examined during February 1984 in the Mountain Zebra National Park in the Eastern Cape Province. Helmeted guineafowls and francolins are not only large birds, but also spend most of their lives on the ground, factors that both probably contribute to their success as hosts of the immature stages of A. marmoreum. Ticks were collected from a total of 1 754 small mammals belonging to 11 species, the majority of which were killed for survey purposes (Table 3). Amongst these there were 579 murid rodents and 31 springhares, a very large rodent, all of which were sampled in localities in which tortoises, or oth- er animals harboured A. marmoreum, and yet only two bush Karoo rats were infested, each with a sin- gle larva. This supports the contention of Petney, Horak, Howell & Meyer (2004) that rodents are not good hosts of Amblyomma spp. They arrived at this conclusion after recovering only five unhealthy-look- ing larvae and a nymph of Amblyomma hebraeum from just six of 169 collections made from striped grass mice in a habitat heavily contaminated with 16 South African tortoise tick, Amblyomma marmoreum TABLE 2 Amblyomma marmoreum collected from birds Host species Number examined Number infested Number of ticks collected Larvae Nymphs Males Females Total Helmeted guineafowl, Numida meleagris 231 177 4 175 206 0 0 4 381 Greywing francolin, Francolinus africanus 7 4 129 0 0 0 129 Cape francolin, Francolinus capensis 7 3 15 1 0 0 16 Crested francolin, Francolinus sephaena 23 13 582 10 0 0 592 Swainson’s francolin, Francolinus swainsonii 1 0 0 0 0 0 0 Total 269 197 4 901 217 0 0 5 118 TABLE 1 Amblyomma marmoreum collected from reptiles Host species Number examined Number infested Number of ticks collected Larvae Nymphs Males Females Total Leopard tortoise, Geochelone pardalis 59 56 336 92 301 83 812 Geometric tortoise, Psammobates geometricus 64 54 9 7 52 12 80 Karoo tortoise, Psammobates oculifer 11 11 0 1 9 4 14 Tent tortoise, Psammobates tentorius tentorius 24 11 8 8 14 2 32 Tent tortoise, Psammobates tentorius trimeni 5 1 0 0 1 0 1 Angulate tortoise, Chersina angulata 52 6 0 5 12 1 18 Areolate padloper, Homopus areolatus 73 68 58 63 32 20 173 Speckled padloper, Homopus signatus 11 2 81 0 1 0 82 Greater padloper, Homopus femoralis 4 4 0 1 4 0 5 Karoo padloper, Homopus boulengeri 2 2 2 5 0 0 7 White-throated monitor, Varanus exanthematicus 1 1 0 1 1 0 2 Puff adder, Bitis arietans 2 1 0 0 1 0 1 Gaboon adder, Bitis gabonica 1 0 2 0 0 0 2 Total 309 217 496 183 428 122 1 229 17 I.G. HORAK et al. larvae of this tick. With the exception of scrub hares, of which 43.6 % were infested with A. marmoreum, and which collectively also harboured surprisingly large numbers of nymphs, other small mammals also appeared not to be suitable hosts of this parasite. Fifteen carnivore species, comprising 213 individu- als that were killed for survey and other purposes, were examined. The prevalence of infestation was highest on black-backed jackals (Table 4). The average prevalence of infestation on the 656 herbivores, all of which had been killed for survey purposes, was 28.2 % and varied between 2.4 % on 41 warthogs to 72.7 % on 11 elands (Table 5). The only black wildebeest infested was a very old ani- mal, which harboured a burden of 146 larvae and two nymphs, while 34 infested greater kudus had mean burdens of 92 larvae. With the exception of a single male tick on a bontebok ram examined dur- ing December 1979 in the Bontebok National Park in the Western Cape Province (Horak, Brown, Boom- ker, De Vos & Van Zyl 1982), no large herbiv orous animal was infested with adult ticks. The ticks from domestic cats and dogs were collect- ed either by the staff at veterinary clinics when the animals were brought in for treatment, or by their owners and hence cannot be regarded as complete collections or as a true indication of the prevalence of infestation on these animals. Those collected from horses, cattle, sheep and goats were recov- ered from animals that had been slaughtered for survey purposes and had thus been thoroughly processed for the recovery of external and internal parasites. The ticks recorded on humans were col- lected as part of an on-going survey to identify those species that bite people in South Africa (Horak, Fourie, Heyne, Walker & Needham 2002). The incomplete nature of the collections made from dogs and cats is endorsed by the fact that larger numbers of nymphs than larvae were recovered, whereas on the other domestic animals, for which TABLE 3 Amblyomma marmoreum collected from small mammals Host species Number examined Number infested Number of ticks collected Larvae Nymphs Males Females Total Pouched mouse, Saccostomys campestris 14 0 0 0 0 0 0 Namaqua rock mouse, Aethomys namaquensis 425 0 0 0 0 0 0 Striped grass mouse, Rhabdomys pumilio 91 0 0 0 0 0 0 Swamp rat, Otomys irroratus 2 0 0 0 0 0 0 Bush Karoo rat, Otomys unisulcatus 47 2 2 0 0 0 2 Spring hare, Pedetes capensis 31 0 0 0 0 0 0 Rock dassie, Procavia capensis 102 21 108 3 0 0 111 Rock elephant shrew, Elephantulus myurus 296 7 10 1 0 0 11 Cape hare, Lepus capensis 67 8 15 4 0 0 19 Scrub hare, Lepus saxatilis 623 272 1 260 395 0 0 1 655 Smith’s red rock rabbit, Pronolagus rupestris 56 17 36 3 0 0 39 Total 1 754 327 1 431 406 0 0 1 837 18 South African tortoise tick, Amblyomma marmoreum the collection procedures had been more thorough, the converse was true (Table 6). The two horses that were examined had both been used as trails horses in the Mountain Zebra National Park, where four of 14 Cape mountain zebras and eight of 11 elands examined during the same period were in- fested. The cattle were examined on farms in Valley Bushveld in the Eastern Cape Province (Horak 1999) and in False Upper Karoo in south-western Free State Province (Fourie & Horak 1990), the sheep on farms in Valley Bushveld and Eastern Province Thorn veld (Horak et al. 1991a), and the goats in Valley Bushveld and in Noorsveld in the Eastern Cape Province (Horak et al. 1991d; 2001) and in Mixed Bushveld in Limpopo Province (Boom ker et al. 1994). The prevalence and intensity of infesta- tion was greater on cattle and sheep than on goats, while the intensity of infestation was greater on cat- tle than on sheep (Table 6). Horak et al. (2002) noted that the comparatively small total number of only 194 collections of ticks taken from humans over four decades reflects the tendency in South Africa for individuals and health- care personnel to discard attached specimens, and more particularly larvae, once they have been re moved. In addition, a large proportion of persons living or working in rural environments in the eastern, north- eastern and northern regions of the country regard TABLE 4 Amblyomma marmoreum collected from carnivores Host species Number examined Number infested Number of ticks collected Larvae Nymphs Males Females Total Black-backed jackal, Canis mesomelas 8 8 243 27 0 0 270 Hunting dog, Lycaon pictus 8 1 0 16 0 0 16 Bat-eared fox, Otocyon megalotis 2 1 1 0 0 0 1 Cheetah, Acinonyx jubatus 3 2 26 18 0 0 44 Caracal, Caracal caracal 51 35 1 360 15 0 0 1 375 African wild cat, Felis lybica 1 1 1 0 0 0 1 Lion, Panthera leo 24 17 159 203 0 0 362 Leopard, Panthera pardus 6 5 43 202 0 0 245 Yellow mongoose, Cynictis penicillata 80 3 11 0 0 0 11 White-tailed mongoose, Ichneumia albicauda 2 2 7 0 0 0 7 Banded mongoose, Mungos mungo 2 1 7 0 0 0 7 Spotted hyaena, Crocuta crocuta 10 2 0 15 0 0 15 Aardwolf, Proteles cristatus 1 1 27 0 0 0 27 Civet cat, Civettictis civetta 7 6 16 46 0 0 62 Large-spotted genet, Genetta tigrina 8 6 13 3 0 0 16 Total 213 91 1 914 545 0 0 2 459 19 I.G. HORAK et al. tick-bite as a normal occurrence and would seldom consider retaining specimens. Thus, the eight in- stances of bites by A. marmoreum are likely to rep- resent only a small proportion of bites on humans due to this species. The large numbers of A. marmoreum larvae collect- ed from the vegetation by drag-sampling with flan- nel strips implies that they quest for hosts from this vantage point. This would seem to be an unneces- sary strategy if tortoises and other land-bound rep- tiles are their only hosts. By questing from the vege- tation the larvae are unlikely to be particularly host-specific and will attach to a variety of animals, an observation supported by the present findings. Norval (1975) stated that adult ticks attach in great- er numbers around the bases of the hind-legs of tortoises, and nymphs around those of the forelegs as well as on the head and neck, while larvae are evenly distributed between the two sites. Fielden & Rechav (1994) and Burridge, Simmons & Allan (2000) report most adults on the upper soft-skinned parts of the hind-legs and in the hollows in front of these legs, as well as around the base and on the ventral surface of the tail. Larvae and nymphs at- tach mainly in soft skinned localities that are pro- tected by the carapace, particularly the neck and upper legs (Fielden & Rechav 1994). Uys & Horak (2005) collected equal numbers of A. marmoreum larvae from the bodies and from the wings of crest- TABLE 5 Amblyomma marmoreum collected from large herbivores Host species Number examined Number infested Number of ticks collected Larvae Nymphs Males Females Total Cape mountain zebra, Equus zebra zebra 14 4 180 1 0 0 181 Warthog, Phacochoerus africanus 41 1 2 0 0 0 2 Giraffe, Giraffa camelopardalis 6 1 0 2 0 0 2 Impala, Aepyceros melampus 229 67 2 227 23 0 0 2 250 Black wildebeest, Connochaetes gnou 13 1 146 2 0 0 148 Bontebok, Damaliscus pygargus dorcas 47 14 90 4 1 0 95 Springbok, Antidorcas marsupialis 22 2 4 0 0 0 4 African buffalo, Syncerus caffer 1 1 8 1 0 0 9 Eland, Taurotragus oryx 11 8 167 0 0 0 167 Greater kudu, Trage- laphus strepsiceros 120 34 3 131 2 0 0 3 133 Red forest duiker, Cephalophus natalensis 23 12 40 8 0 0 48 Gemsbok, Oryx gazella 26 15 457 13 0 0 470 Grey rhebok, Pelea capreolus 62 20 210 4 0 0 214 Reedbuck, Redunca arundinum 21 2 12 0 0 0 12 Mountain reedbuck, Redunca fulvorufula 20 3 10 2 0 0 12 Total 656 185 6 684 62 1 0 6 747 20 South African tortoise tick, Amblyomma marmoreum ed francolins, fewer from their tails and the least from their heads and upper necks. They suggest that this attachment pattern might be a strategy to avoid competition with the larvae of A. hebraeum and Hyalomma marginatum rufipes, of which more than 84 % attach to the heads and upper necks of the birds. Seasonality The countrywide seasonality of all stages of devel- opment of A. marmoreum on tortoises is graphically illustrated in Fig. 1. Male and female ticks were most numerous on tor- toises during January and February. Thereafter, with the exception of July, the only month during which female ticks outnumbered males, the numbers of female ticks remained low even when the numbers of males started to increase on tortoises from Octo- ber to December. Norval (1975) recorded the largest numbers of adult ticks on leopard tortoises on a farm in the Eastern Cape Province from January to March, whereas Rechav & Fielden (1995) recorded the largest numbers of adults on these animals in the National Zoological Gardens, Pretoria from Octo- ber to January, with males most numerous from October to May and females from September to December. Female ticks can take up to 60 days (Norval 1975) to 91 days (Fielden et al. 1992) to complete feeding on artificially infested tortoises, and Dower et al. (1988) recorded a period as long as 73 days before all females and 111 days before all males had de- tached from tortoises that they had collected in the field. The January and February peak in adult tick numbers may therefore reflect an accumulation of ticks that had attached a month or two earlier. The longer period of attachment of male ticks may in part explain the preponderance of male compared to female ticks on tortoises. Larvae were most numerous on tortoises, irrespec- tive of the localities in which they had been sam- pled, during March (Fig. 1), and on helmeted guinea- fowls and cattle in inland Valley Bushveld in the Eastern Cape Province from February to April with an April peak on the guineafowls and a March peak on the cattle (Fig. 2A and B). Larvae were most nu- merous on helmeted guineafowls, scrub hares and the vegetation in the Lowveld of north-eastern TABLE 6 Amblyomma marmoreum collected from domestic animals and from humans Host species Number examined Number infested Number of ticks collected Larvae Nymphs Males Females Total Dogs 915 8 2 13 0 0 15 Cats 20 1 0 2 0 0 2 Horses 2 2 14 0 0 0 14 Cattle 58 32 1 942 17 0 0 1 959 Sheep 175 81 1 132 30 0 0 1 162 Goats 373 82 851 73 0 0 924 Humans 194 7 2 3 3 0 8 Total 1 737 213 3 943 138 3 0 4 084 FIG. I The seasonal occurrence of Amblyomma marmoreum on tortoises in South Africa ��������� �� �� ������������� � � � �� � � � � � � �� �� �� � � � ��� �� ��� � �� � �� ��� � � � � � � � � � � � � � � � � � ! � �� 21 I.G. HORAK et al. ��������� �� �� ��� "#�$� %�&��'() ����$(* �� � � � � �� � � � � � � �� �� � � � � � � �� � � � � � � � � ! � � � �� � � � � � � �� �� �� �� � � �� �� �� �� �� �� � �� �� � � � � � � �� � �� ��� � �� �� � �� � � �� � �� �� �� �� �� � � �� � � � ��������� �� �� �����+�#,(� ���'(-�. ! �� �� �� �� �� �� �� � � � �� � � � � � � � � ! � �� � �� ��� ��������� �� �� ��� ��"�� ���$'(-�. ) � �� � � � � � � � � ! � �� � � � � �� � � � � � � �� �� �� �� � � �� �� �� �� �� �� �� � ��������� �� �� ����+ ����'() ����$(* �� / � � � �� � � � � � � �� �� � � � � � � � � �� � � � � � � �� �� �� �� � � ��� ��� ��� ��� ��� �� � �� �� �� �� �� � � � �� � � � � � � � � ! � �� � �� ��� � � � �� � � � � � � �� �� � � � � � � � � �� � � � � � � �� �� �� �� � � ��������� �� �� ����"#�$� %�&��'(-�. * ��� �� �� �� �� � �� � � � � � � �� � � � � � � � � ! � �� � �� ��� FIG. 2 The seasonal occurrence of the larvae and nymphs of Amblyomma marmoreum on (A) helmeted guinea fowls and (B) domestic cattle in Valley Bushveld in the East- ern Cape Province, and (C) helmeted guineafowls, and (D) scrub hares, and of larvae on (E) vegetation in the Lowveld of north-eastern Mpumalanga Province. KNP = Kruger National Park 22 South African tortoise tick, Amblyomma marmoreum Mpumalanga Province from March or April to June or July, with peaks in May (Fig. 2C–E). Very few if any larvae were present from October to December or January in either of the provinces. Norval (1975) collected most larvae from a naturally infested leop- ard tortoise during April and from the vegetation on a farm in the Eastern Cape Province from February to June with a peak in May. Rechav & Fielden (1995) recorded the largest numbers of larvae on tortoises in the National Zoological Gardens, Pretoria from January to May with a peak in February and March. Nymphs were most numerous on tortoises, irrespec- tive of the localities in which they had been exam- ined, during April (late summer) and during Sep tem- ber (spring) (Fig. 1). Nymphs were most numerous on helmeted guineafowls and on cattle in inland Valley Bushveld from September to December (Fig. 2A and B), and on scrub hares in the Lowveld from October to December (Fig. 2D). However, nymphs were most numerous on guineafowls in the latter habitat from December to August (Fig. 2C). The largest numbers of nymphs were present on tortois- es in the National Zoological Gardens, Pretoria from May to October with a peak in June and July (Rechav & Fielden 1995). Compared to 1 604 larvae, only six nymphs were collected during nearly 14 years of monthly drag- sampling the vegetation in the Lowveld. These nymphs have not been incorporated in Fig. 2E. On the other hand, Norval (1975) collected 449 larvae and 27 nymphs from the vegetation by this sam- pling method and the latter were most numerous from October to January. The present results indi- cate that the seasonal pattern of occurrence of the immature stages of A. marmoreum in the north-east of the country is similar to that in the south-east. Norval (1975) thought that hosts other than tortois- es did not play a significant role in the life cycle or seasonality of A. marmoreum because of the small number of ticks he encountered on these hosts. However, the substantial numbers presently record- ed on some host species, other than tortoises, as well as the proportion of these animals that are in- fested, imply that they may well play an important role in the tick’s life cycle. In his experiments on the life cycle of A. marmoreum Norval (1975) found that larvae required up to 30 days to complete feeding on tortoises and nymphs up to 51 days, whereas larvae he fed on the ears of sheep engorged in 6–12 days and nymphs in 8–20 days. Dower et al. (1988) recorded a mean of 35 days and a range of 8–104 days for larvae, and a mean of 21 days and range of 4–47 days for nymphs to detach from tortoises col- lected in the field. As there was no way of knowing exactly how many days before capture these ticks attached to the latter tortoises, all these periods are probably considerably longer. Fielden et al. (1992) compared the length of the life cycle of A. marmoreum on tortoises and on guinea pigs in the laboratory. On tortoises the period be- tween larval attachment and the emergence of adults varied between 69 and 172 days, whereas on guinea pigs it varied between 63 and 95 days. Domestic chickens, and hence presumably guinea- fowls, have higher body temperatures than those of mammals, and larvae of A. hebraeum fed on chick- ens engorged and detached in 4–8 days compared to 5–10 days on rabbits infested at the same time (Holley & Petney 1988). If a similar phenomenon occurs when the immature stages of A. marmoreum feed on guineafowls as opposed to sheep, the length of the life cycle could be reduced even further. According to Norval (1975) the life cycle of A. mar- moreum in the Eastern Cape Province can be com- pleted in either 1 or 2 years. He proposed that for it to be completed in 1 year, it was necessary for lar- vae to feed on tortoises in late summer and the re- sultant nymphs and subsequent adults to feed on tortoises in spring and in early summer respectively. Fielden et al. (1992) suggest that host selection by the immature stages could be important in deter- mining whether the life cycle is completed in 1 or in 2 years, an opinion with which we concur. Provided the larvae and the nymphs feed on mammals or birds in late summer and in spring respectively and the adults on tortoises in early summer the life cycle can be completed in 1 year. Geographic distribution Theiler & Salisbury (1959) mapped the distribution of A. marmoreum in South Africa from the geo- graphic coordinates of 49 localities at which collec- tions were made. We have now added more than 100 localities to their map (Fig. 3). Most collections have been made in the western re- gions of the Western and Eastern Cape and Free State provinces, and in the north-eastern regions of the Northern Cape, KwaZulu-Natal, Mpumalanga and Limpopo provinces. The seemingly large number of localities at which A. marmoreum was present in north-eastern Mpumalanga and Limpopo provinces are a reflection of the numerous surveys conducted in these regions by Horak and his co-workers over a period of 25 years. The several collections made in other regions imply that these are also suitable hab- 23 I.G. HORAK et al. itats for the tick. Very few collections of A. mar- moreum have been made in the eastern Highveld regions of the Eastern Cape, Free State and Mpu- ma langa provinces and inland mountainous regions of KwaZulu-Natal. We are, however, convinced that future collections will indicate an even wider distri- bution for A. marmoreum in South Africa than that now proposed. ACKNOWLEDGEMENTS We are indebted to Mr P.D. Burdett who was re- sponsible for many of the tick collections from rep- tiles, and thank the South African National Parks for placing the animals as well as their staff and facili- ties in the various National Parks at our disposal. We gratefully acknowledge the assistance of Messrs C. Cheney, J. Sithole, M.M. Knight, E.J. Williams and the late B.D. De Klerk with processing the car- casses of the survey animals for the recovery of ectoparasites, and that of Mrs E.L. Visser, Miss M. L. Horak, Mr A.C. Uys and Mr E.J. Williams who as- sisted with the recovery of ticks from the processed material. Dr R. Williams of the Onderstepoort Vet- erinary Institute constructed the distribution map. REFERENCES ALLAN, S.A., SIMMONS, L.-A. & BURRIDGE, M.J. 1998. Establishment of the tortoise tick Amblyomma marmoreum (Acari: Ixodidae) on a reptile-breeding facility in Florida. Jour- nal of Medical Entomology, 35:621–624. BEZUIDENHOUT, J.D. 1987. Natural transmission of heartwater. Onderstepoort Journal of Veterinary Research, 54:349–351. BEZUIDENHOUT, J.D. 1988. Sekere aspekte van hartwater oor- draging, voorkoms van die organisme in bosluise en in vitro kweking. D.V.Sc. thesis, University of Pretoria. BOOMKER, J., HORAK, I.G. & RAMSAY, K.A. 1994. Helminth and arthropod parasites of indigenous goats in the northern Transvaal. Onderstepoort Journal of Veterinary Research, 61:13–20. BURRIDGE, M.J., SIMMONS, L.-A. & ALLAN, S.A. 2000. Intro- duction of potential heartwater vectors and other exotic ticks into Florida on imported reptiles. Journal of Parasitology, 86: 700–704. BURRIDGE, M.J. 2001. Ticks (Acari:Ixodidae) spread by the inter national trade in reptiles and their potential roles in dis- semination of diseases. Bulletin of Entomological Research, 91:3–23. BURRIDGE, M.J. & SIMMONS, L.A. 2003. Exotic ticks intro- duced into the United States on imported reptiles from 1962 to 2001 and their potential roles in international dissemina- tion of diseases. Veterinary Parasitology, 113:289–320. DOWER, KATHY M., PETNEY, T.N. & HORAK, I.G. 1988. The developmental success of Amblyomma hebraeum and Amblyomma marmoreum on the leopard tortoise, Geochelone FIG. 3 The geographic distribution of Amblyomma marmoreum within the borders of South Africa 24 South African tortoise tick, Amblyomma marmoreum pardalis. Onderstepoort Journal of Veterinary Research, 55: 11–13. FIELDEN, L.J., MAGANO, S. & RECHAV, Y. 1992. Laboratory studies on the life cycle of Amblyomma marmoreum (Acari: Ixodidae) on two different hosts. Journal of Medical Ento mol- ogy, 29:750–756. FIELDEN, L.J. & RECHAV, Y. 1994. Attachment sites of the tick Amblyomma marmoreum on its tortoise host, Geochelone pardalis. Experimental and Applied Acarology, 18:339–349. FOURIE, L.J. & HORAK, I.G. 1990. Parasites of cattle in the south western Orange Free State. Journal of the South African Veterinary Association, 61:27–28. HOLLEY, A.D. & PETNEY, T.N. 1988. The use of domestic chick- ens as laboratory hosts of the larvae of the bont tick, Ambly- omma hebraeum. Onderstepoort Journal of Veterinary Re- search, 55:75–76. HORAK, I.G., BROWN, MOIRA R., BOOMKER, J., DE VOS, V. & VAN ZYL, ELSA A. 1982. Helminth and arthropod para- sites of blesbok, Damaliscus dorcas phillipsi, and of bonte- bok, Damaliscus dorcas dorcas. Onderstepoort Journal of Veterinary Research, 49:139–146. HORAK, I.G. & FOURIE, L.J. 1986. Parasites of domestic and wild animals in South Africa. XIX. Ixodid ticks and fleas on rock dassies (Procavia capensis) in the Mountain Zebra National Park. Onderstepoort Journal of Veterinary Research, 53:123–126. HORAK, I.G., MACIVOR, K.M., PETNEY, T.N. & DE VOS, V. 1987a. Some avian and mammalian hosts of Amblyomma hebraeum and Amblyomma marmoreum (Acari: Ixodidae). Onderstepoort Journal of Veterinary Research, 54:397–403. HORAK, I.G., JACOT GUILLARMOD, AMY, MOOLMAN, L.C. & DE VOS, V. 1987b. Parasites of domestic and wild animals in South Africa. XXII. Ixodid ticks on domestic dogs and on wild carnivores. Onderstepoort Journal of Veterinary Re- search, 54:573–580. HORAK, I.G., WILLIAMS, E.J. & VAN SCHALKWYK, P.C. 1991a. Parasites of domestic and wild animals in South Africa. XXV. Ixodid ticks on sheep in the north-eastern Orange Free State and in the eastern Cape Province. Onderstepoort Journal of Veterinary Research, 58:115–123. HORAK, I.G., FOURIE, L.J., NOVELLIE, P.A. & WILLIAMS, E.J. 1991b. Parasites of domestic and wild animals in South Africa. XXVI. The mosaic of ixodid tick infestations on birds and mammals in the Mountain Zebra National Park. Onder- stepoort Journal of Veterinary Research, 58:125–136. HORAK, I.G., SPICKETT, A.M., BRAACK, L.E.O. & WILLIAMS, E.J. 1991c. Parasites of domestic and wild animals in South Africa. XXVII. Ticks on helmeted guineafowls in the eastern Cape Province and eastern Transvaal Lowveld. Onderstepoort Journal of Veterinary Research, 58:137–143. HORAK, I.G., KNIGHT, M.M. & WILLIAMS, E.J. 1991d. Parasites of domestic and wild animals in South Africa. XXVIII. Helminth and arthropod parasites of Angora goats and kids in Valley Bushveld. Onderstepoort Journal of Veterinary Research, 58:253–260. HORAK, I.G. & FOURIE, L.J. 1991. Parasites of domestic and wild animals in South Africa. XXIX. Ixodid ticks on hares in the Cape Province and on hares and red rock rabbits in the Orange Free State. Onderstepoort Journal of Veterinary Research, 58:261–270. HORAK, I.G., BOOMKER, J., SPICKETT, A.M. & DE VOS, V. 1992. Parasites of domestic and wild animals in South Africa. XXX. Ectoparasites of kudus in the eastern Transvaal Low- veld and the eastern Cape Province. Onderstepoort Jour nal of Veterinary Research, 59:259–273. HORAK, I.G., SPICKETT, A.M., BRAACK, L.E.O. & PENZHORN, B.L. 1993. Parasites of domestic and wild animals in South Africa. XXXII. Ixodid ticks on scrub hares in the Transvaal. Onderstepoort Journal of Veterinary Research, 60:163–174. HORAK, I.G. & BOOMKER, J. 1998. Parasites of domestic and wild animals in South Africa. XXXV. Ixodid ticks and bot fly larvae in the Bontebok National Park. Onderstepoort Journal of Veterinary Research, 65:205–211. HORAK, I.G. 1999. Parasites of domestic and wild animals in South Africa. XXXVII. Ixodid ticks on cattle on Kikuyu grass pastures and in Valley Bushveld in the Eastern Cape Prov- ince. Onderstepoort Journal of Veterinary Research, 66:175– 184. HORAK, I.G., BRAACK, L.E.O., FOURIE, L.J. & WALKER, JANE B. 2000. Parasites of domestic and wild animals in South Africa. XXXVIII. Ixodid ticks collected from 23 wild carnivore species. Onderstepoort Journal of Veterinary Research, 67: 239–250. HORAK, I.G., MACIVOR, K.M. DE F. & GREEFF, C.J. 2001. Parasites of domestic and wild animals in South Africa. XXXIX. Helminth and arthropod parasites of Angora goats in the southern Karoo. Onderstepoort Journal of Veterinary Re- search, 68:27–35. HORAK, I.G., FOURIE, L.J., HEYNE, HELOISE, WALKER, JANE B. & NEEDHAM, G.R. 2002. Ixodid ticks feeding on humans in South Africa: with notes on preferred hosts, geo- graphic distribution, seasonal occurrence and transmission of pathogens. Experimental and Applied Acarology, 27:113– 136. HORAK, I.G., GALLIVAN, G.J., BRAACK, L.E.O., BOOMKER, J. & DE VOS, V. 2003. Parasites of domestic and wild animals in South Africa. XLI. Arthropod parasites of impalas (Aepy- ceros melampus) in the Kruger National Park. Onderstepoort Journal of Veterinary Research, 70:131–163. HORAK, I.G. & MATTHEE, SONJA 2003. Parasites of domestic and wild animals in South Africa. XLIII. Ixodid ticks of domes- tic dogs and cats in the Western Cape Province. Onderstepoort Journal of Veterinary Research, 70:187–195. NORVAL, R.A.I. 1975. Studies on the ecology of Amblyomma marmoreum Koch 1844 (Acarina: Ixodidae). Journal of Para- sitology, 61:737–742. NORVAL, R.A.I. 1983. The ticks of Zimbabwe. VII. The genus Am blyomma. Zimbabwe Veterinary Journal, 14:292–305. OBEREM, P.T. & BEZUIDENHOUT, J.D. 1987. Heartwater in hosts other than domestic ruminants. Onderstepoort Journal of Veterinary Research, 54:271–275. PETER, T.F., BURRIDGE, M.J. & MAHAN, S.M. 2000. Com- petence of the African tortoise tick Amblyomma marmoreum (Acari: Ixodidae), as a vector of the agent of heartwater (Cowdria ruminantium). Journal of Parasitology, 86:438– 441. PETNEY, T.N., HORAK, I.G., HOWELL, D.J. & MEYER, S. 2004. Striped mice, Rhabdomys pumilio, and other murid rodents as hosts for immature ixodid ticks. Onderstepoort Journal of Veterinary Research, 71:313–318. RECHAV, Y. & FIELDEN, L.J. 1995. Seasonal abundance of the tortoise tick Amblyomma marmoreum (Acari: Ixodidae) on the leopard tortoise. Journal of Medical Entomology, 32:161– 165. SPICKETT, A.M., HORAK, I.G., VAN NIEKERK, ANDREA & BRAACK, L.E.O. 1992. The effect of veld-burning on the seasonal abundance of free-living ixodid ticks as determined 25 I.G. HORAK et al. by drag-sampling. Onderstepoort Journal of Veterinary Re- search, 59:285–292. THEILER, GERTRUD 1943. Ticks in the South African Zoological Survey Collection. Part II. Onderstepoort Journal of Veterinary Science and Animal Industry, 18:85–89. THEILER, GERTRUD & SALISBURY, LOIS E. 1959. Ticks in the South African Zoological Survey Collection—Part IX—“The Amblyomma marmoreum group”. Onderstepoort Journal of Veterinary Research, 28:47–124. UYS, A.C. & HORAK, I.G. 2005. Ticks on crested francolins, Francolinus sephaena and on the vegetation on a farm in Limpopo Province, South Africa. Onderstepoort Journal of Veterinary Research, 72:339–343. WALKER, JANE B. & SCHULZ, K.C.A. 1984. Records of the bont tick, Amblyomma hebraeum, from the angulate tortoise, Chersina angulata, and the leopard tortoise, Geochelone par- dalis. Onderstepoort Journal of Veterinary Research, 51: 171–173. WALKER, JANE B. & OLWAGE, A. 1987. The tick vectors of Cowdria ruminantium (Ixodoidea, Ixodidae, genus Ambly- omma) and their distribution. Onderstepoort Journal of Vet- erinary Research, 54:353–379. << /ASCII85EncodePages false /AllowTransparency false /AutoPositionEPSFiles true /AutoRotatePages /None /Binding /Left /CalGrayProfile (Dot Gain 20%) /CalRGBProfile (sRGB IEC61966-2.1) /CalCMYKProfile (U.S. Web Coated \050SWOP\051 v2) /sRGBProfile (sRGB IEC61966-2.1) /CannotEmbedFontPolicy /Error /CompatibilityLevel 1.4 /CompressObjects /Tags /CompressPages true /ConvertImagesToIndexed true /PassThroughJPEGImages true /CreateJDFFile false /CreateJobTicket false /DefaultRenderingIntent /Default /DetectBlends true /DetectCurves 0.0000 /ColorConversionStrategy /CMYK /DoThumbnails false /EmbedAllFonts true /EmbedOpenType false /ParseICCProfilesInComments true /EmbedJobOptions true /DSCReportingLevel 0 /EmitDSCWarnings false /EndPage -1 /ImageMemory 1048576 /LockDistillerParams false /MaxSubsetPct 100 /Optimize true /OPM 1 /ParseDSCComments true /ParseDSCCommentsForDocInfo true /PreserveCopyPage true /PreserveDICMYKValues true /PreserveEPSInfo true /PreserveFlatness true /PreserveHalftoneInfo false /PreserveOPIComments true /PreserveOverprintSettings true /StartPage 1 /SubsetFonts false /TransferFunctionInfo /Apply /UCRandBGInfo /Preserve /UsePrologue false /ColorSettingsFile () /AlwaysEmbed [ true ] /NeverEmbed [ true ] /AntiAliasColorImages false /CropColorImages true /ColorImageMinResolution 300 /ColorImageMinResolutionPolicy /OK /DownsampleColorImages true /ColorImageDownsampleType /Bicubic /ColorImageResolution 1200 /ColorImageDepth -1 /ColorImageMinDownsampleDepth 1 /ColorImageDownsampleThreshold 1.00000 /EncodeColorImages true /ColorImageFilter /DCTEncode /AutoFilterColorImages true /ColorImageAutoFilterStrategy /JPEG /ColorACSImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /ColorImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /JPEG2000ColorACSImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /JPEG2000ColorImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /AntiAliasGrayImages false /CropGrayImages true /GrayImageMinResolution 300 /GrayImageMinResolutionPolicy /OK /DownsampleGrayImages true /GrayImageDownsampleType /Bicubic /GrayImageResolution 1200 /GrayImageDepth -1 /GrayImageMinDownsampleDepth 2 /GrayImageDownsampleThreshold 1.00000 /EncodeGrayImages true /GrayImageFilter /DCTEncode /AutoFilterGrayImages true /GrayImageAutoFilterStrategy /JPEG /GrayACSImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /GrayImageDict << /QFactor 0.15 /HSamples [1 1 1 1] /VSamples [1 1 1 1] >> /JPEG2000GrayACSImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /JPEG2000GrayImageDict << /TileWidth 256 /TileHeight 256 /Quality 30 >> /AntiAliasMonoImages false /CropMonoImages true /MonoImageMinResolution 1200 /MonoImageMinResolutionPolicy /OK /DownsampleMonoImages true /MonoImageDownsampleType /Bicubic /MonoImageResolution 1200 /MonoImageDepth -1 /MonoImageDownsampleThreshold 1.00000 /EncodeMonoImages true /MonoImageFilter /CCITTFaxEncode /MonoImageDict << /K -1 >> /AllowPSXObjects false /CheckCompliance [ /None ] /PDFX1aCheck false /PDFX3Check false /PDFXCompliantPDFOnly false /PDFXNoTrimBoxError true /PDFXTrimBoxToMediaBoxOffset [ 0.00000 0.00000 0.00000 0.00000 ] /PDFXSetBleedBoxToMediaBox true /PDFXBleedBoxToTrimBoxOffset [ 0.00000 0.00000 0.00000 0.00000 ] /PDFXOutputIntentProfile (None) /PDFXOutputConditionIdentifier () /PDFXOutputCondition () /PDFXRegistryName () /PDFXTrapped /False /Description << /CHS /CHT /DAN /DEU /ESP /FRA /ITA /JPN /KOR /NLD (Gebruik deze instellingen om Adobe PDF-documenten te maken die zijn geoptimaliseerd voor prepress-afdrukken van hoge kwaliteit. De gemaakte PDF-documenten kunnen worden geopend met Acrobat en Adobe Reader 5.0 en hoger.) /NOR /PTB /SUO /SVE /ENU (Use these settings to create Adobe PDF documents best suited for high-quality prepress printing. Created PDF documents can be opened with Acrobat and Adobe Reader 5.0 and later.) /ENS () >> /Namespace [ (Adobe) (Common) (1.0) ] /OtherNamespaces [ << /AsReaderSpreads false /CropImagesToFrames true /ErrorControl /WarnAndContinue /FlattenerIgnoreSpreadOverrides false /IncludeGuidesGrids false /IncludeNonPrinting false /IncludeSlug false /Namespace [ (Adobe) (InDesign) (4.0) ] /OmitPlacedBitmaps false /OmitPlacedEPS false /OmitPlacedPDF false /SimulateOverprint /Legacy >> << /AddBleedMarks false /AddColorBars false /AddCropMarks false /AddPageInfo false /AddRegMarks false /ConvertColors /ConvertToCMYK /DestinationProfileName () /DestinationProfileSelector /DocumentCMYK /Downsample16BitImages true /FlattenerPreset << /PresetSelector /MediumResolution >> /FormElements false /GenerateStructure false /IncludeBookmarks false /IncludeHyperlinks false /IncludeInteractive false /IncludeLayers false /IncludeProfiles false /MultimediaHandling /UseObjectSettings /Namespace [ (Adobe) (CreativeSuite) (2.0) ] /PDFXOutputIntentProfileSelector /DocumentCMYK /PreserveEditing true /UntaggedCMYKHandling /LeaveUntagged /UntaggedRGBHandling /UseDocumentProfile /UseDocumentBleed false >> ] >> setdistillerparams << /HWResolution [1200 1200] /PageSize [595.276 841.890] >> setpagedevice