Ticks (Acari: Ixodidae) spread by the international trade in reptiles and their potential roles in dissemination of diseases

The international trade in live reptiles has grown dramatically in the last decade. Since many of these reptiles are infested with ticks, the number of ticks introduced to new exotic locations has also increased. This is causing concern in importing countries such as the United States because some of the reptilian ticks are known to be vectors of diseases of veterinary and economic importance, such as heartwater. Rational measures to control these tick species and to eradicate new introductions have been slow to develop due in part to the scattered and often obscure sources of available data on the exotic ticks. This review is an attempt to collate information on the geographical distribution, host range, life cycle and associations with diseases for four Amblyomma species, A. marmoreum Koch, A. nuttalli D?nitz, A. sparsum Newmann, and for four Aponomma species, A. exornatum (Koch), A. flavomaculatum (Lucas), A. latum (Koch)( and A. varanensis (Supino), that have recently been introduced into Florida, USA on imported reptiles.     

Evidence of Cowdria ruminantium infection (heartwater) in Amblyomma sparsum ticks found on tortoises imported into Florida

Amblyomma marmoreum and A. sparsum ticks were collected from tortoises imported into Florida from Africa and were tested for Cowdria ruminantium infection using a C. ruminantium-specific pCS20 polymerase chain reaction assay. In I shipment imported from Zambia, 15 of the 38 A. sparsum male ticks collected from the leopard tortoises (Geochelone pardalis) were found to be positive for infection with C. ruminantium. In contrast, all 148 A. marmoreum tested were negative for C. ruminantium infection. This is the first reported evidence of the introduction of heartwater-infected ticks into the United States, but there were no opportunities to confirm isolation of C. ruminantium from the ticks by either culture or transmission studies.     

Importation of Exotic Ticks into the United Kingdom via the International Trade in Reptiles

Due to the increased trade in exotic reptiles, many of which are infested with ticks of various genera, there is an increased risk of exotic ticks and pathogens being introduced and potentially becoming established in new geographical areas. Despite the number and variety of tick species collected from reptiles, their role in the maintenance of pathogens and transmission to humans has not been fully investigated for all species. The potential public health risks to the United Kingdom have been examined through a preliminary study involving the collection and identification of exotic tick species imported via the reptile trade. Reptiles imported into Heathrow Airport, London (July 2003–October 2004) were carefully examined for ectoparasites. Five species of tick were collected: Aponomma exornatum, Ap. latum, Amblyomma rotundatum, Am. dissimile and Am. nuttalli. This is the first report of Am. dissimile identified from an interception at Heathrow airport. The potential for establishment of exotic ticks in the UK and the public health risks are discussed.     

Phylogeny of the hard ticks (Ixodidae) inferred from 18S rRNA indicates that the genus Aponomma is paraphyletic

We examined the phylogeny of ticks (Acari:Parasitiformes:Ixodida) and their closest known mite relatives (Acari:Parasitiformes:Mesostigmata and Holothyrida) using 18S rRNA sequences. In our analyses, we included sequences from 36 taxa. Sequences for 13 hard ticks (Family Ixodidae), 5 soft ticks (Family Argasidae), and 2 mesostigmatid mites were obtained from the GenBank database and we generated sequences for 15 hard ticks and 1 holothyrid mite. Ten of these tick species were endemic to Australia. Our analyses indicated that the suborder Holothyrida is more closely related to Ixodida than to Mesostigmata, the group used as outgroup in earlier molecular studies. This finding is consistent with Lehtinen's (1991) hypothesis that the Holothyrida rather than the Mesostigmata is the sister-group to the Ixodida. Within the hard ticks the genus Aponomma and thus the family Amblyomminae were paraphyletic. Taxonomic revision of these taxa is needed. The genus Amblyomma was paraphyletic without the inclusion of "typical" Aponomma species (Ap. latum and Ap. fimbriatum). There was a basal divergence between endemic Australian and other species in both the Metastriata and the Prostriata divisions of the hard ticks.     

Competence of the African tortoise tick, Amblyomma marmoreum (Acari: Ixodidae), as a vector of the agent of heartwater (Cowdria ruminantium)

The ability of the African tortoise tick, Amblyomma marmoreum, to acquire and transmit Cowdria ruminantium infection was investigated experimentally with transmission trials and with a C. ruminantium-specific polymerase chain reaction (PCR) detection assay. Laboratory-reared A. marmoreum larvae and nymphs were fed on small ruminants with clinical heartwater. After molting, the resultant nymphs were fed on Cowdria ruminantium-naive sheep (n = 3), and the adults were ground and inoculated intravenously into sheep (n = 5). Fatal heartwater developed in the 5 recipient animals, demonstrating larvae-nymph transmission and nymph-adult acquisition of infection. Cowdria ruminantium infection was also detected in adult A. marmoreum by PCR analysis, although at lower frequency (10%) than in Amblyomma hebraeum ticks (43%), the major vector of C. ruminantium in southern Africa, which had been fed simultaneously on the infected animals (P<0.0001). Amblyomma marmoreum, therefore, can be an effective vector of C. ruminantium. The potential role of this species in heartwater epidemiology and in the spread of the disease to new areas is highlighted by these results and by the fact that immature stages of this tick feed readily on domestic and wild animals susceptible to C. ruminantium.     

Amblyomma marmoreum on tortoises of southern province, Zambia

Reptiles from Southern Province, Zambia were captured and inspected for ticks. Seven of 18 tortoises (Geochelone pardalis) were infested by small numbers of adults and nymphs of Amblyomma marmoreum. Under such circumstances, the tick had little apparent effect on the host. None of the 13 specimens representing four species of snakes examined were infested with ticks.     

Acquired immunity to larvae of Amblyomma marmoreum and Ahebraeum by tortoises, guinea-pigs and guinea-fowl

A study of acquired resistance in guinea-pigs, guinea-fowl and tortoises to larvae of the ticks Amblyomma hebraeum Koch and A.marmoreum Koch (Acari: Ixodidae) showed that repeated infestations of the laboratory host resulted in a 29.3-49.4% reduction respectively in weight of engorged larvae. No resistance was induced in guinea-fowl, the natural host for larvae of both species. A small decline in the mean weight of engorged larvae was observed for both species of ticks after three successive infestations on tortoises. The reduction in weight was more pronounced in A.hebraeum (14.5%) which does not naturally feed on tortoises than for A.marmoreum (8.4%), a common tick on this host. The occurrence of acquired resistance in natural tick host relationships as opposed to unnatural tick host relationships is discussed.     

Host-seeking behaviour by Australian ticks (Acari: Ixodidae) with differing host specificities

Ticks generally detach from their hosts into sites where they are later exposed to host species which may or may not be suitable for infestation. The question of how four species of ixodid ticks, with differing specificities, behave towards such potential host species was examined. Observations of the generalists,Aponomma hydrosauri andAmblyomma limbatum and the specialists,Aponomma fimbriatum andAponomma concolor, showed that the generalists were attracted to a wider range of potential host species than the specialists and that the larval stages of all tick species, regardless of specificity, contacted more potential host species than the adults. The interspecific differences may be attributed to reliance on different sets of host cues, while the intraspecific differences may reflect the developmental state of the sensory system.     

Ant predation on different life stages of two Australian ticks

Laboratory colonies of Rhytidoponera ants were allowed to prey on the fed and unfed stages of the Australian ticks Aponomma hydrosauri and Amblyomma limbatum. The unfed tick stages had a higher survival than the fed stages. The ants took longer to handle the adult ticks than the nymphs and longer to handle the nymphs than the larvae. The ants also took longer to handle the unfed than fed nymphs, but longer to handle the fed than unfed females. As well as the differences between the tick stages, there was a species effect, with the ants taking longer to handle A. limbatum, and with that tick species having a higher survival than A. hydrosauri after ant predation. These stage and species differences may influence the tick population dynamics. This revised version was published online in November 2006 with corrections to the Cover Date.     

Influence of temperature and relative humidity on the moulting success of Amblyomma limbatum and Aponomma hydrosauri (Acari: Ixodidae) larvae and nymphs

This study compared the duration of the moulting periods of engorged larvae and nymphs of the ixodid ticks, Amblyomma limbatum and Aponomma hydrosauri, at different temperature/relative humidity regimes, and examined the relationships between the engorged weight of ticks and their weights after moulting. The results showed that for each species, there was a significant relationship between the weights of unfed nymphs and engorged larvae, and the weights of unfed adults and engorged nymphs. The weight of engorged nymphs was also a good indicator of their sex, with female ticks having heavier weights as engorged nymphs. Temperature and relative humidity had a marked effect on the moulting success of engorged ticks of both species. Aponomma hydrosauri larvae and nymphs were able to moult at lower temperatures than Amb. limbatum but most ticks, except Ap. hydrosauri larvae, failed to moult at 13 degrees C. Additionally, there was a marked decrease in the pre-moult times of ticks at higher temperatures, with larvae taking less time to moult than nymphs. At temperatures greater than 21 degrees C, Amb. limbatum took less time to moult than Ap. hydrosauri but this interspecific difference was less marked for nymphs. The interspecific differences in the responses of engorged larvae and nymphs to different temperatures and relative humidities correlated with interspecific differences in off-host behaviour and with the different climates the two species experience throughout most of their distributional range.     

Ticks parasitizing reptiles in the Bahamas

Two species of reptile ticks, Amblyomma dissimile Koch and Amblyomma torrei Pérez Vigueras (Acari: Ixodidae), are reported from the Bahama Islands for the first time. The widespread neotropical (including the Caribbean and southern Florida) A. dissimile was recovered on Andros Island from three species of reptiles all for the first time: the Andros iguana Cyclura cychlura cychlura Cuvier, the Andros curly tail lizard Leiocephalus carinatus coryi Schmidt, and the Andros boa Epicrates striatus fowleri Sheplan and Schwartz. The iguana tick A. torrei, previously known only from Cuba, Puerto Rico and the Cayman Islands, was recovered in the Exuma Islands from the Exuma iguana Cyclura cychlura figginsi Barbour. Mean numbers of ticks per host were as high as 36.6 on Mangrove Cay, Andros Island, and 25.8 on Pasture Cay in the Exuma Islands.     

Geographic occurrence of Ixodes scapularis and Amblyomma americanum (Acari: Ixodidae) infesting white-tailed deer in North Carolina

A state-wide survey to determine the occurrence and comparative numbers of ticks infecting white-tailed deer (Odocoileus virginianus) was conducted in North Carolina (USA). One thousand six hundred twenty nine deer were examined in 60 of 100 counties; with the exception of one county in the piedmont region, all tick-infested deer occurred in the coastal plain. Ixodes scapularis (46%) and Amblyomma americanum (53%) were the most prevalent species encountered and accounted for more than 98% of the 4,286 ticks collected. Some specimens of Dermacentor albipictus and Amblyomma maculatum also were collected.     

Borrelia sp. in ticks recovered from white-tailed deer in Alabama.

Six hundred sixty-five hunter-killed white-tailed deer (Odocoileus virginianus) from 18 counties in Alabama (USA) were examined for ticks. Most of the collections were made at state-operated wildlife management areas. Four species of ticks (n = 4,527) were recovered: the lone star tick Amblyomma americanum (n = 482); the Gulf Coast tick A. maculatum (n = 11); the winter tick Dermacentor albipictus (n = 1,242); and the black-legged tick Ixodes scapularis (n = 2,792). Fifty-six percent of the ticks (n = 2,555) were examined for Borrelia sp. spirochetes using an immunofluorescent, polyclonal antibody assay. Spirochetes were detected in I. scapularis (five females, seven males) from Barbour, Butler, Coosa, and Lee counties and A. americanum (four males, four nymphs) from Hale, Lee, and Wilcox counties. Area-specific prevalences in ticks were as high as 3.3% for I. scapularis and 3.8% for A. americanum.     

A re-evaluation of relationships in the Metastriata (Acari: Parasitiformes: Ixodidae)

A systematic analysis of generic/subgeneric relationships in the ixodid lineage Metastriata was conducted based on 82 structural and developmental characters, 15 of which have multiple states. Results of the analysis show considerable agreement with current classifications of the Ixodidae, including good support for monophyly of the Metastriata, the genera Ixodes and Haemaphysalis, and the grouping of Hoogstraal's Rhipicephalinae and Hyalomminae, and fair support for the genus Hyalomma. Our results differ from these classifications most notably by rejecting monophyly of the genera Aponomma and Amblyomma. Instead, the analysis provides weak support for a hypothesis in which the basal two to three lineages in the Metastriata are all composed of Aponomma species, and in which a fourth lineage within that genus, Aponomma elaphense, clusters with Amblyomma quadricavum to form a more derived lineage. Resolution is insufficient to support or reject monophyly of the genera Dermacentor and Rhipicephalus, or to resolve the position of the genus Haemaphysalis relative to the other Metastriata. Overall resolution within the Rhipicephalinae/Hyalomminae is quite good, but it is quite poor among the Amblyomminae and Haemaphysalinae. These results are similar to the results of recent 16S and 18S rDNA based molecular analyses. There are few indications of host specificity among the lineages analysed. The basal metastriate lineages contain a large number of squamate associates, but the pattern is not sufficiently clear to reject the hypothesis that these ticks will feed on all available vertebrate hosts. On the other hand, nearly all of the basal taxa are Australian. This suggests a possible origin of the Metastriata in Australia, with subsequent dispersal to other parts of the world.     

The coevolution of ixodid ticks and terrestrial vertebrates

Paleontologic and zoogeographic data speak in favour of Mesozoic origin of ixodid ticks. The absence of strict restrictions for the feeding on unusual species of hosts has caused the domination of polyphagy and oligophagy over monophagy among ixodid ticks. The same peculiarities of ixodid ecology are responsible for a restricted part or absence of phylogenetic parallelism with hosts in their evolution. Primary food relations with reptiles are, apparently, preserved only in the genus Aponomma and in many species of Amblyomma while hosts for most species of other genera are mammals and, to a lesser extent, birds. The number of potential hosts in these species can be much greater than that of real ones. Restrictions in the distribution of some species are connected rather with direct effect of unfavourable environmental factors on their nonparasitic stages of the life cycle than with the absence of suitable hosts. During the evolution of natural landscapes and at a shorter stages under the influence of successions or anthropogenic factors ixodids easily adapt themselves to feeding on new species of hosts. So the differentiation of primary and secondary hosts of these parasites is rather difficult.     

Bird ticks in an area of the Cerrado of Minas Gerais State, southeast Brazil

In the present study the tick prevalence, mean intensity of infestation and species were recorded on birds captured between January 2009 and December 2010 in the Ecological Station Pirapitinga-ESEC from Minas Gerais State, Brazil. A total of 967 birds, from 15 families and 40 species were captured and 165 (17.1 %) individuals were parasitized by ticks. Of these 160 (97 %) belonged to the order Passeriformes. Five tick species were identified: Amblyomma longirostre (n = 274) was the most common species followed by Amblyomma parvum (n = 43), Amblyomma nodosum (n = 39), Amblyomma ovale (n = 24) and Riphicephalus sanguineus (n = 7). None of 61 unengorged larvae molted to nymph. The mean intensity of infestation was 2.7 ± 2.4 ticks per bird (448 ticks/165 birds) ranging from 1 to 10. Only 19 (11.4 %) birds were infested with one species of tick. The remaining birds were infested by two, three or four species of ticks. Also new hosts for all five ticks were recorded. Only nymphs were recorded throughout the year with two similar peaks during autumn and winter 2009 and 2010.     

Ticks (Acari: Ixodidae) from yellow armadillo, Euphractus sexcinctus (Cingulata: Dasypodidae), in Brazil's Pantanal wetlands

Tick species parasitizing yellow armadillo, Euphractus sexcinctus, were recorded from October 2006 to October 2007 in Pantanal. A total of 89 ticks were collected from 23 yellow armadillos. Most ticks (n=50) were identified as Amblyomma cajennense (Fabricius) (32 males and 18 females). The only other species found was Amblyomma parvum (Arag?o) (three females and two males). The remaining ticks were immatures of Amblyomma (29 nymphs and five larvae). The prevalence of A. cajennense was 55%, the mean intensity was 2.7±0.5 (SE) (n=17) and the mean abundance was 1.5±0.4 (n=31).     

Interspecific differences in the movements of female ticks on reptiles.

Movements of females of two reptile ticks, Amblyomma limbatum and Aponomma hydrosauri were studied to determine whether the behaviour of the species on hosts was similar or different. Experiments were conducted to determine if the movement of females on hosts prior to mating was influenced by the delayed attachment of conspecific males. A field experiment was also undertaken to determine whether data obtained during laboratory experiments reflected the behaviour of females on hosts in the field. Both in laboratory and field experiments, a significantly greater proportion of Ap. hydrosauri females changed their site of attachment prior to mating. Individual Ap. hydrosauri females made significantly more positional changes than Amb. limbatum females. These interspecific differences occurred irrespective of the absence of conspecific males or presence of non-conspecific adults on hosts. These data may have important ecological implications in relation to the success of colonizing females at their parapatric boundary.     

Exotic ectoparasites of ostriches recently imported into the United States

Eleven species of ectoparasitic arthropods were collected and identified from ostriches (Struthio camelus) recently imported into the United States from Africa and Europe. Four of these species are reported from ostriches for the first time. The parasites included adult hippoboscid flies (Struthiobosca struthionis) and 10 species of adult ixodid ticks (Amblyomma gemma, A. lepidum, A. variegatum, Haemaphysalis punctata, Hyalomma albiparmatum, H. luscitanicum, H. marginatum rufipes, H. truncatum, Hyalomma sp., and Rhipicephalus turanicus. As a result of these findings, the U.S. Department of Agriculture prohibited further importation into the United States of ostriches and other flightless birds on an interim basis.