INTRODUCTION OF POTENTIAL HEARTWATER VECTORS AND OTHER EXOTIC TICKS INTO FLORIDA ON IMPORTED REPTILES

Since 1962, there have been a number of reports of exotic ticks being introduced into the United States on imported animals. The majority of the infested animals were mammals (Diamant, 1965; Becklund, 1968; Anderson et al., 1984; Burridge, 1997) and birds (Mertins and Schlater, 1991), but a few have been reptiles (Becklund, 1968; Anderson et al., 1981, 1984; Wilson and Barnard, 1985; Allan et al., 1998). Actions were taken by United States regulatory authorities to modify rules regarding importation of mammals and birds (Mertins and Schlater, 1991) that resulted in control of introduction of exotic ticks on these animals. However, no such actions have been taken with regard to reptiles, and as a consequence, increased numbers of exotic ticks are gaining entry to the United States on imported reptiles. A 3-mo surveillance exercise that began in November 1994 at Miami International Airport, a principal port of entry for reptiles into the United States, found ticks on 28% of the 349 imported shipments examined (Clark and Doten, 1996). Soon thereafter, the African tortoise tick Amblyomma marmoreum was identified outside importation facilities in central Florida on a reptile-breeding premises, and subsequent investigations confirmed that this exotic tick had become established on that site (Allan et al., 1998).

These findings in Florida demonstrated that there was a flow of exotic ticks into the United States, and these ticks included species of major potential economic concern, such as the tick A. marmoreum that has been shown to be an efficient experimental vector of heartwater, a lethal rickettsial disease of ruminants (Peter et al., 2000). This raised several questions, including the extent to which the exotic ticks were being disseminated within Florida. The present paper describes a preliminary study undertaken to determine the extent of the dissemination of exotic ticks within reptile facilities in Florida as a prerequisite to an assessment of their impact on animal and human health and the development of methods for their control.

MATERIALS AND METHODS

RESULTS

All 11 major importers in Florida were found to have reptiles infested with 1 or more species of exotic ticks. Exotic ticks were found also in reptile-breeding facilities, zoos, wildlife theme parks, pet stores, wildlife care centers, and collections of private hobbyists (Table I). Eight species of exotic ticks were identified. Included were 4 Amblyomma species (A. marmoreum, A. nuttalli, A. sabanerae, and A. sparsum) and 4 Aponomma species (A. exornatum, A. flavomaculatum, A. latum, and A. varanensis). Reptiles from a total of 32 premises were examined, and on 29 (91%) of these sites from 18 counties, a variety of tortoises, snakes, and monitor lizards were found to be infested with exotic ticks (Table II).

Table I. Exotic ticks found on imported reptiles in Florida by type of premises, 1997–1999

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Table II. Hosts of exotic ticks found in Florida

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The most frequently encountered exotic species was the snake tick A. latum, with 724 adults and nymphs found on 215 reptiles, all but 3 of which were snakes. By far the most common host for A. latum was the ball python (Python regius), with 568 ticks on 202 hosts. Aponomma latum adults and nymphs were found attached to all body parts of the snakes. However, the most common attachment site was the head, with some found even attached in the periorbital recess under the eye. On tortoises, A. latum attached to the head and, on monitors, in the nasal cavities and ear canals.

The second most frequently encountered exotic tick was the African tortoise tick A. marmoreum, with 460 individuals found on 114 tortoises and 3 dogs. This tick was found primarily on 2 species, the leopard tortoise Geochelone pardalis and the African spurred tortoise Geochelone sulcata, with 9 premises infested in 6 different counties of Florida. Many of the engorging A. marmoreum females were enormous in size, with the largest measuring 2.7 cm long by 1.4 mm wide and weighing 4.66 g. The preferred attachment site for A. marmoreum adults on tortoises was the upper soft-skinned parts of the rear legs, whereas, in contrast, nymphs and larvae were always found on the anterior part of the tortoises, especially the neck and axillae.

The other 6 species of exotic ticks found on imported reptiles were present in small numbers on a variety of reptiles (Table II). Adults of the small reptile tick A. nuttalli were attached to the head of the snakes, to the forelegs of the tortoises, and to the belly of the monitor. The adults of the neotropical tortoise tick A. sabanerae found on tortoises were attached to their head or forelegs. Adults of the large reptile tick A. sparsum were attached to the feet or lower legs of the tortoises. Adults of the monitor lizard tick A. exornatum were attached to the head and legs of the monitors and to the head of the snake. The adults of the yellow-spotted monitor lizard tick A. flavomaculatum were attached in the nasal cavities and ear canals and on the belly and toes of monitors, and on both the head and body of snakes, whereas the nymphs were found engorging on the head of a monitor. Finally, the adults of the Asian monitor tick A. varanensis found on the snake were attached to its head.

DISCUSSION

The results of the present study show that there is a population of exotic ticks in Florida on imported reptiles. Furthermore, the results suggest that the exotic ticks are being disseminated from importers to breeders, zoos, wildlife theme parks, pet stores, and private hobbyists. What is not known yet is whether or not these exotic tick infestations are spreading to the native Floridian fauna. However, the potential for such spread is very real because not only are exotic ticks widespread in Florida on imported reptiles, but at least 1 species, the African tortoise tick A. marmoreum, had formed a breeding colony on the premises of a reptile breeder (Allan et al., 1998). The geographical distribution of A. marmoreum has been limited to continental southern Africa (Theiler and Robinson, 1954; Walker, 1991), and yet ticks from the breeding colony in Florida had already spread to 1 species of imported tortoise from South America (the yellow-footed tortoise Geochelone denticulata), 1 from islands in the Pacific Ocean (the Galapagos tortoise Geochelone elephantopus), and 1 from islands in the Indian Ocean (the Aldabra giant tortoise Geochelone gigantea), as well as to native domestic dogs. Furthermore, in the present study the African tick A. nuttalli was found on a common boa (Boa constrictor) from Latin America, the African tick A. exornatum on a water monitor (Varanus salvator) from Asia, the African tick A. latum on a yellow-footed tortoise from South America and on a reticulated python (Python reticulatus) from southeast Asia, and the Asian tick A. varanensis on a ball python from West Africa. These findings demonstrate clearly the potential for at least 5 of the exotic reptilian ticks to spread rapidly in Florida, not only to other reptilian species, but in the case of 1 also to domestic animals such as dogs.

An extensive search of the scientific literature has shown that little is known about the 8 exotic tick species that have recently been imported into Florida on reptiles, especially regarding their capacity to act as disease vectors. Only 4 of these ticks have been associated with disease, A. marmoreum (Peter et al., 2000) and A. sparsum (Norval and Mackenzie, 1981) with heartwater, and A. nuttalli (Babudieri, 1959; Arthur, 1962) and A. exornatum (Arthur, 1962) with Q fever.

The most worrisome importation is associated with A. marmoreum because it has been shown to be an efficient vector of heartwater (Peter et al., 2000), which is an acute tickborne disease of domestic and wild ruminants caused by the rickettsia Cowdria ruminantium. If introduced into the United States, heartwater would be expected to cause mortality of from 40 to 100% in susceptible host species such as cattle, sheep, goats, and deer (Burridge, 1997). Although A. marmoreum is a reptilian tick with adults feeding primarily on tortoises, snakes, and lizards (Theiler and Salisbury, 1959), its immature larval and nymphal stages will feed on ruminants susceptible to heartwater, including cattle, sheep, and goats (Theiler and Salisbury, 1959; MacLeod, 1975; Horak and Knight, 1986; Horak et al., 1987; Fivaz et al., 1990; Horak, Knight, and Williams, 1991; Horak, Williams, and van Schalkwyk, 1991) and wild antelope such as the African buffalo Syncerus caffer (Jack, 1942), the eland Taurotragus oryx (Horak et al., 1987; Horak, Fourie et al., 1991), and the kudu Tragelaphus strepsiceros (Horak and Knight, 1986; Horak et al., 1987, 1992). Consequently, it is possible that A. marmoreum ticks could become infected with heartwater as immatures in southern Africa and then be imported into the United States on reptiles as infected nymphs or adults.

Allan et al. (1998) have already shown that imported A. marmoreum ticks can become established into a breeding colony in Florida and that these exotic ticks can then spread to other reptiles and domestic animals within the infested premises. In the absence of control measures, spread of A. marmoreum beyond the infested premises is likely, given the predilection of the tick for tortoises, snakes, and lizards (Theiler and Salisbury, 1959) and for birds in its immature stages (Norval, 1975; Horak et al., 1987), all of which are abundant in Florida. The present study suggests that A. marmoreum ticks are being introduced into Florida in large numbers through reptile importers and, from there, are being disseminated at least to breeders, zoos, and wildlife theme parks. The situation is optimal for the widespread establishment of A. marmoreum within the wild fauna of Florida, with spillover to domestic animals, and the threat that this poses to the cattle, sheep, and goat industries and to the deer and exotic hoofstock populations of the United States through the introduction and establishment of heartwater, is very real.

Another worrisome importation is that of A. sparsum, because it too has been shown to be a vector of heartwater (Norval and Mackenzie, 1981). Unlike the other reptilian ticks found on imported reptiles in this study, A. sparsum also commonly infests large mammals such as the African buffalo (Norval and Mackenzie, 1981; Walker and Olwage, 1987), a known carrier of heartwater (Andrew and Norval, 1989). Hence, it is not only possible that A. sparsum ticks could be imported into the United States infected with heartwater, but, if they were to become established, they could parasitize heartwater-susceptible ruminants such as African buffalo that are found in many wildlife collections in the United States. Amblyomma sparsum has been recorded once before in the United States on an African ball python (P. regius) found in a pet shop in Tennessee (Durden and Kollars, 1992).

Two of the exotic tick species found on reptiles imported into Florida have been reported to be susceptible to Coxiella burnetii, the rickettsial agent causing Q fever in humans. These are the small reptile tick A. nuttalli and the monitor lizard tick A. exornatum. Amblyomma nuttalli has been reported to harbor natural infections of C. burnetii (Babudieri, 1959; Arthur, 1962), as has A. exornatum (Arthur, 1962). An outbreak of Q fever that occurred in New York in 1978 was associated with the handling and removal of ticks (A. nuttalli, A. latum, and A. flavomaculatum) from a shipment of ball pythons from Ghana (Kim et al., 1978). However, no C. burnetii organisms were isolated from either the pythons or the exotic ticks they were carrying, and therefore, there is no direct evidence of any causal association between the ticks and the outbreak of Q fever. Furthermore, of these 2 ticks, only A. nuttalli has been reported to feed on humans (Theiler and Salisbury, 1959; Morel, 1961; Morel and Finelle, 1961; Aeschlimann, 1967; Cornet, 1995).

Whereas only A. marmoreum has been reported to have established in Florida (Allan et al., 1998), there is every reason to believe that the climate of Florida would be suitable to maintain the other 7 exotic species of ticks imported into the state that originate from tropical and subtropical areas of Africa (A. nuttalli, A. sparsum, A. exornatum, A. flavomaculatum, and A. latum), Asia (A. varanensis), and Central America (A. sabanerae). Furthermore, there is an abundance of suitable indigenous reptilian species in Florida to maintain all 8 tick species. Consequently, continuation of unregulated importation of reptiles will lead, in all likelihood, to the establishment of breeding colonies of all the exotic species, with unknown consequences for the native fauna of Florida. Earlier this century, other exotic reptilian ticks were introduced into Florida and became established, becoming indigenous tick species. Examples include the iguana tick Amblyomma dissimile (Bequaert, 1932) and the rotund toad tick Amblyomma rotundatum (Oliver et al., 1993), demonstrating the ease with which exotic tick species can become indigenous when import controls are lacking.

In addition to the 8 exotic tick species identified in the present study, the nymph of a ninth exotic species, the tropical bont tick Amblyomma variegatum, was identified in 1997 on a savanna monitor (Varanus exanthematicus) in a shipment to a reptile importer in Florida (N. L. Cardenas, pers. comm.). This report is particularly significant because A. variegatum is associated with a number of diseases of both veterinary and public health significance to the United States. It is the most widespread vector of heartwater in Africa and the Caribbean (Walker and Olwage, 1987). It also is closely associated in both the Caribbean and Africa with a horrific skin disease of cattle, acute bovine dermatophilosis (Burridge et al., 1984; Koney et al., 1996) and is associated with the newly recognized human rickettsial disease, African tick-bite fever (Parola et al., 1998). Clearly A. variegatum must not be allowed to become established in the United States.

It might be expected that ticks would be readily visible on reptiles, especially given the relatively large size of many of these exotic tick species. However, this is not always the case, especially with A. marmoreum, A. exornatum, and A. flavomaculatum and, on occasion, A. latum. Preferred attachment sites for A. marmoreum on tortoises are body areas protected from contact with the shell or outside objects (Fielden and Rechav, 1994) and these are typically under the shell on the soft-skinned upper parts of the legs. These sites are not visible except by manual extension of the legs of the tortoise, and typically owners of tortoises infested with A. marmoreum are not even aware of the infestations. One of the common sites of attachment of A. exornatum and A. flavomaculatum to monitors is the nasal cavities (Hesse, 1985; Norval, 1985; Williams and Bayless, 1998), and in the present study, A. flavomaculatum and A. latum were found in both the nasal cavities and ear canals of monitors. Some A. latum adults were found partially hidden, feeding in the periorbital recess of ball pythons and could only be detached by pulling down the skin under the eye of the snakes. It is clear, therefore, that some ticks species cannot be detected by a cursory examination of reptilian hosts.

The results of the present study demonstrate that exotic tick species are present in Florida on imported reptiles and that, once introduced, these ticks can be widely disseminated throughout the state. This ease of dissemination is not surprising when it is realized that these tick species can take months to feed on a reptilian host. For example, A. marmoreum adults can take up to 111 days to detachment (Dower et al., 1988), and A. sparsum adults can take up to 62 days to become fully engorged on tortoises (Walker and Parsons, 1964). What is not clear at this time is the extent to which these exotic tick infestations have spread to the native fauna and what impact such spread might have on both domestic and wild animal populations in Florida. There is the possibility that these exotic ticks may carry pathogens that could have a negative impact on indigenous American hosts. However, we do know that 3 species found on imported reptiles (A. marmoreum, A. sparsum, and A. variegatum) are vectors of heartwater and that 1 of them (A. marmoreum) has become established on at least 1 premises in Florida. Actions must be taken to control the flow of exotic ticks into Florida on imported reptiles, and we are working on practical solutions to this complex problem.