Hosts, seasonality and geographic distribution of the South African tortoise tick, Amblyomma marmoreum.

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 Numberexamined
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 Numberexamined
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 Numberexamined
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