First Reports of Ectoparasites Collected From Wild-Caught Exotic Reptiles in Florida

Abstract

We collected ectoparasites from 27 of 51 wild-caught, free-ranging exotic reptiles examined in Florida from 2003 to 2008. Sampled animals represented eight species, five of which yielded ectoparasites. Reported new parasite distribution records for the United States include the following: the first collection of the African tick Amblyomma latum (Koch) from a wild-caught animal [ball python, Python regius (Shaw)] in the United States; the first collection of the lizard scale mite Hirstiella stamii (Jack) from any wild-caught animal [green iguana, Iguana iguana (L.)]; and the first collection of the lizard scale mite Geckobia hemidactyli (Lawrence) in the continental United States from a wild-caught tropical house gecko, Hemidactylus mabouia (Moreau de Jonnès). We also report the first collections of the Neotropical ticks Amblyomma rotundatum (Koch) and Amblyomma dissimile (Koch) from wild-caught Burmese pythons, Python molurus bivittatus (Kuhl); the first collections of A. dissimile from a wild-caught African savannah monitor, Varanus exanthematicus (Bosc); and from wild-caught green iguanas in the United States; and the first collections of the native chiggers Eutrombicula splendens (Ewing) and Eutrombicula cinnabaris (Ewing) from wild-caught Burmese pythons. These reports may only suggest the diversity of reptile ectoparasites introduced and established in Florida and the new host–parasite relationships that have developed among exotic and native ectoparasites and established exotic reptiles.

Amblyomma dissimile, Amblyomma latum, Amblyomma rotundatum, Geckobia hemidactyli, Hirstiella stamii

In recent decades, the keeping of small, exotic animals as pets has gained extreme popularity worldwide. As part of this trend, captive exotic reptile imports into the United States reached ≈1.7 million animals annually in 1970. Such live reptile imports declined after the 1973 passage of the U.S. Endangered Species Act and the 1975 agreement to the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), but in the 1990s, trade in live reptiles again began to increase. In 1995, ≈2.5 million live reptiles were legally imported into the United States (Hoover 1998), and in 2000–2004, the mean number of documented reptile imports per year was 1.8 million (Jenkins et al. 2007).

Many instances of tick infestations on imported animals, including reptiles, have been reported from the United States in the past. Becklund (1968) first reviewed quarantine and other records through 1968 and found that 37 tick species had been collected from foreign livestock, zoo animals, animal products, and other imported items. Subsequently, Strickland et al. (1976), Anderson et al. (1981, 1984), Wilson and Barnard (1985), and the U.S. National Tick Surveillance Program (NTSP, e.g., USDA 1994) periodically reported and discussed a continuing recurrence of exotic tick interceptions in the United States.

A more recent summary of exotic tick records from interceptions made at U.S. ports of entry between 1958 and 1997 (Wilson and Bram 1998) documented numerous occurrences of 23 different species, including some reptile ticks. Furthermore, Wilson and Bram (1998) documented other instances of some of the same exotic ticks, plus five more species, detected beyond quarantine conditions on domestic premises in 14 states. Keirans and Durden (2001) reviewed and summarized published and unpublished records from several federal tick systematic collections and listed at least 99 exotic tick species that had been either detected at ports of entry or inadvertently imported into the United States during the second half of the twentieth century. Burridge and Simmons (2003) reviewed and summarized information for 29 species of exotic ticks that were reported previously (1962–2001) as introduced into the United States specifically on captive imported reptiles.

Routine monitoring of ticks on imported animals by the NTSP (unpublished records) made pivotal discoveries when it identified Amblyomma sparsum Neumann collected in 1991 by the Southeastern Cooperative Wildlife Disease Study (SCWDS) in South Carolina from imported Tanzanian tortoises, and the same tick species was detected again in Florida from a Varanus sp. monitor lizard imported in 1994. These findings led to a targeted, active survey for ticks on imported herpetological specimens at the Miami (FL) International Airport in 1994–1995 (Clark and Doten 1996). Over a 3-mo period, animals were inspected from 117,690 imported reptiles and amphibians in 349 shipments from 22 countries; ticks were collected from one or more animals in 97 shipments that included 54,376 animals. Thirteen species of ticks were encountered, including four collections of another African tortoise tick Amblyomma marmoreum (Koch). Both A. sparsum and A. marmoreum are experimental African vectors of the rickettsial agent of heartwater (Norval and Mackenzie 1981, Peter et al. 2000), a fatal disease of ruminants.

In 1997, Allan et al. (1998) found an established population of A. marmoreum at an outdoor exotic reptile breeding facility in central Florida. In a subsequent survey of captive exotic reptiles at various facilities in Florida (Burridge et al. 2000a), eight species of exotic ticks were identified on animals at 29 of 32 (91%) suspect premises visited in 18 counties.

Many of these surveillance and monitoring activities and summaries, especially those of Clark and Doten (1996), Wilson and Bram (1998), Burridge et al. (2000a), Burridge and Simmons (2003), suggest a potential for serious consequences from the presence of exotic ticks on imported herpetological pets. Ticks entering the United States on imported animals may be spread from importers to breeders, zoos, wildlife parks, pet stores, or private collectors (Burridge 2001), and they could become established at these sites, in the surrounding environment, or at distant sites, if infested hosts escape or are released into the environment. Moreover, these ticks might be carrying foreign disease agents that could be spread among captive animals via trade, or introduced into native wildlife, domestic animals, or even humans, if the ticks escape into the environment.

Out of concern over this scenario, we began collecting ectoparasites from free-ranging exotic reptiles in Florida in 2003, as part of a larger survey for exotic arthropods of livestock on wildlife in the southeastern United States. We report herein both exotic and native ectoparasites collected for the first time over a 6-yr period from wild-caught, free-ranging exotic reptiles in Florida.

Materials and Methods

We sought after wild-caught exotic reptiles in Florida from 2003 to 2008. We captured free-ranging reptiles in several standard ways, including by hand, via live traps (Havahart, Lititz, PA, and Tomahawk Live Trap Co., Tomahawk, WI), herp poles, and silt fences with tunnel traps. In addition, we examined wild-caught reptiles submitted to wildlife rehabilitation clinics and received ticks collected from wild-caught reptiles by cooperators at other wildlife rehabilitation clinics. From 2003 to 2008, we examined 51 wild-caught exotic reptiles representing eight species: one ball python, Python regius (Shaw); nine brown anoles, Anolis sagrei (Duméril and Bibron); 14 Burmese pythons, Python molurus bivittatus (Kuhl); 1 giant ameiva, Ameiva ameiva (L.); 16 green iguanas, Iguana iguana (L.); four Nile monitors, Varanus niloticus (L.); one savannah monitor, Varanus exanthematicus (Bosc); and five tropical house geckos, Hemidactylus mabouia (Moreau de Jonnès).

Captured reptiles were restrained manually, examined visually, and all ectoparasites seen were collected, stored in 70% ethanol, and identified at the U.S. Department of Agriculture, Animal and Plant Health Inspection Service, Veterinary Services, National Veterinary Services Laboratories (NVSL), Ames, IA. Representative voucher specimens for each ectoparasite species collected are deposited in the parasitology reference collection at the NVSL.

Results and Discussion

We gathered ectoparasites from 27 of the 51 examined wild-caught exotic reptiles (Table 1). There are 28 entries in the table because one green iguana bore two species of ectoparasites. Of the seven ectoparasite species encountered, three are new to the continental United States, and five provide new host records.

Table 1.

Ectoparasites collected from wild-caught exotic reptiles in Florida, 2003–2008^a

We report the first collection of the tick Amblyomma latum (Koch) (Acari: Ixodidae) from a wild-caught ball python in the United States (Table 1). This snake was captured by a private citizen at a residential premises on 11 June 2005, taken to a wildlife rehabilitation clinic cooperating in our survey for exotic ectoparasites, and two ticks were removed from the snake 2 d later. Based on clinic husbandry practices and the absence of ticks on other resident animals, clinic personnel are certain that the snake arrived with the ticks. We note the following circumstances of this collection: the original capture site is within a forested residential area, and an exotic reptile dealer, unrelated to the person that captured the snake, lived and kept exotic reptiles within one km of the capture site. A. latum is a common parasite of large snakes in sub-Saharan Africa and widespread in the pet trade worldwide (Burridge et al. 2000a, Burridge and Simmons 2003). It was the second-most common tick found by Clark and Doten (1996) in their survey of ticks on reptiles imported into Florida, and it has been found previously on captive snakes in many other states (Burridge and Simmons 2003) but never on a wild-caught animal. The ball python is endemic to forested and savanna habitats in a broad band across West and Central Africa; it is a frequent host of this tick there (Burridge et al. 2000a) and is abundant in the international pet trade. CITES parties reported annual numbers (1983–1994) of ball pythons moving in world trade between 6,745 and 166,178 (Hoover 1998). These snakes were the second-most numerous reptiles entering at Miami during the Clark and Doten (1996) survey, and they ranked second-most imported nationally in another study during 1998–2002 (Schlaepfer et al. 2005). We know of no feral breeding populations of ball pythons or A. latum in Florida.

We report the first collection of the mite Hirstiella stamii (Jack) (Prostigmata: Pterygosomatidae) from wild-caught green iguanas (Table 1) and its first collection in the Western Hemisphere. The original description and only previous published report of this mite is from captive green iguanas at the Amsterdam Zoological Gardens in The Netherlands (Jack 1961). Hirstiella is a genus of 12 species of lizard scale mites found in both the New and Old worlds (Paredes-León and Morales-Malacara 2009). Green iguanas are endemic to the neotropics, where they are very common in a variety of habitats and occur widely from southern Mexico through Central America to central South America and on many Caribbean islands (King and Krakauer 1966). They first colonized Miami, FL, in or before 1964, probably from released pet animals, but they may have taken up residence in the state even earlier, in the 1950s in the Florida Keys (Meshaka et al. 2004, Green Iguana Society 2009). Feral breeding populations currently are known in five South Florida counties (FFWCC 2010b). Hoover (1998) cites growing numbers of green iguanas imported annually to the United States, from 142,000 in 1970 to >1.1 million in 1995, and during 1991–1995, they were by far the most numerous imported reptile species, at >3.4 million animals (annual mean = 689,000). Green iguanas also were the most imported reptiles in the Clark and Doten (1996) survey at Miami, but during 1998–2002, they dropped to fifth place nationally (Schlaepfer et al. 2005), at a mean annual number of 60,000 animals. The NTSP also has identified, independent of our survey, a more recent (2007) collection (accession 509608) of H. stamii from a feral green iguana at the Miami Metrozoo, Miami-Dade Co., establishing a second known locality for its existence in the state.

We report the first collection of the mite Geckobia hemidactyli (Lawrence) (Prostigmata: Pterygosomatidae) from the tropical house gecko in the continental United States (Table 1). The genus Geckobia includes >65 species, and each one typically infests either a single species or a small group of species of geckos; G. hemidactyli occurs in Africa on the Tasman's house gecko, Hemidactylus tasmani (Hewitt), and the tropical house gecko (Bochkov and Mironov 2000). This mite was first documented in the Western Hemisphere by Martinez Rivera et al. (2003) from specimens collected on live hosts in Puerto Rico, but previous informal reports existed, and an examination of museum-preserved hosts (Martinez Rivera et al. 2003) found and identified numerous other, older collection localities in South America and the Caribbean. The only temporal data given for these collections indicate that G. hemidactyli existed in Puerto Rico as early as 1972, but five archived house gecko collections examined from Florida were mite-free. The tropical house gecko is native to Africa and was first reported in Florida in 1990, but it probably was present even earlier (Lawson et al. 1991, Meshaka et al. 1994). It is now broadly distributed pantropically and has colonized the southern parts of North America, plus Central and South America (Federico and Cacivio 2000). Martinez Rivera et al. (2003) speculate that G. hemidactyli probably accompanied their introduced house gecko hosts nearly everywhere they established. Hemidactylus spp. were among the most numerous reptiles encountered in the Clark and Doten (1996) survey and ranked first nationally in the Schlaepfer et al. (2005) survey of imported reptiles.

We report here the first collection of the tick Amblyomma rotundatum (Koch) (Acari: Ixodidae) from a wild-caught Burmese python (Table 1). This tick is native to Mexico, Central and South America, and it occurs on several islands in the Caribbean (Guglielmone et al. 2003). Throughout its range, it commonly feeds on reptiles and amphibians, particularly toads and other species in damp habitats (Burridge and Simmons 2003). It became established in Florida sometime during the mid-20th century in association with the introduction of a frequent natural host, the giant toad [Rhinella marina (L.)] from South America (Oliver et al. 1993). Burmese pythons are native to Southeast Asia and were first reported established in southern Florida in the 1980s (Meshaka et al. 2000, 2004, FFWCC 2010a, USGS 2010). Although ≈300,000 individual pythons were imported to the United States in the past 30 yr (Reed and Rodda 2009), most of those arrived early on. In recent years, domestic demand for pet Burmese pythons increasingly has been met by captive U.S.-bred stock. The several A. rotundatum collection records in Table 1 are not surprising, given the preference of both this Neotropical tick and this Asian python for damp habitats, their adoptive coexistence in the Florida Everglades, and the tick's wide herpetological host range.

Although not a part of our current survey, NVSL and the NTSP have older collection records and voucher specimens of A. rotundatum ticks from other wild hosts, both endemic and exotic, in Florida dating between 1991 and 2000. Hosts include giant toads (accession 85456), unspecified toads (92-35074, 92-45407, 97-11952, 97-11955), an unspecified frog (91-27412), an unspecified native turtle (98-13617), and a human (unengorged tick, 93-26240). Counties of origin for these specimens include Broward, Miami-Dade, Palm Beach, and possibly Lee. We have other records (2000 and 2001, respectively) and specimens from both a native cottonmouth, Agkistrodon piscivorus Lacépède (accession 62171), and native canebrake rattlesnakes, Crotalus horridus atricaudatus Garman (112656), in an outdoor herpetarium in Broward Co. More recently (2005), we have identified collections of female A. rotundatum from both a gopher tortoise, Gopherus polyphemus Daudin (accession 402748), and a giant toad (402749) in Fort Lauderdale, Broward Co., and Hanson et al. (2007) document a female A. rotundatum on a wild-caught southern black racer, Coluber constrictor priapus Dunn and Wood, in the Florida Keys, Monroe Co., FL.

We also report here the first collection of the Neotropical reptile tick Amblyomma dissimile (Koch) (Acari: Ixodidae) from a wild-caught Burmese python (Table 1). A. dissimile parasitizes many species of reptiles and amphibians in the West Indies and from Mexico south to Argentina (Jones et al. 1972, Guglielmone et al. 2003). It may have been introduced one or more times into Florida with any of the numerous species of Neotropical reptiles now living free in the state (Meshaka et al. 2004, King 2006), but published early collection records (Bequaert 1932, Jones et al. 1972) suggest that A. dissimile may be endemic or at least may have been present for decades (i.e., since at least 1909) before the more recent onslaught of exotic reptile introductions. Burridge and Simmons (2003) review historical introductions of A. dissimile on imported reptiles into 31 other states plus the District of Columbia, and it was the most frequently encountered tick in the Clark and Doten (1996) survey of imported reptiles at Miami. Because of its broad reptilian host range, this tick easily accepts non-Neotropical reptiles as hosts, and some have been documented (Bequaert 1932, Wilson and Kale 1972, Foster et al. 2000), including at least eight species of native North American snakes and a native tortoise. In this context, parasitism of a feral Asian host in North America by this Neotropical tick is not unpredictable.

We further report the first collection of A. dissimile from a wild-caught savannah monitor (Table 1). The savannah monitor is native to most of the sub-Saharan Sahel Region of Africa (Bayless 2002), but it has not yet been reported as established in Florida (Meshaka et al. 2004, Owens et al. 2005). This monitor was the fourth most numerous species encountered by Clark and Doten (1996) in their survey of imported reptiles at Miami and also in import numbers nationally during 1991–1995 (Hoover 1998). Once again, the broad host range of A. dissimile renders its North American acceptance of and occurrence on a feral African lizard unsurprising.

Perhaps least surprising of the A. dissimile records we report is its collection on feral green iguanas in Florida (Table 1). Knowledge of this host-parasite connection in the neotropics traces back to the earliest biological studies of A. dissimile, and “iguana tick” is an early, unofficial common name used for it (Hooker et al. 1912, Dunn 1918). Although free-ranging green iguanas in Florida surely must have been subject to A. dissimile parasitism since their initial occurrence, as far as we can determine, ours is the first published observation of the phenomenon in the continental United States. In fact, unpublished presurvey identification records from the SCWDS and NTSP contain documentation (NVSL accessions 99-2378, 99-4887, 99-4890) and specimens of many A. dissimile females, males, nymphs, and larvae collected by one of us (JLC) from six feral iguanas at Estero, Lee Co., FL, on 15 October 1998. The NTSP also has identified, independent of our survey, a more recent (2007) collection (accession 509608) of A. dissimile from a feral green iguana at the Miami Metrozoo, confirming the continuing existence of both the lizards and the ticks at this locality.

In Table 1, we report the first collections of two chigger mite species (Prostigmata: Trombiculidae) from wild-caught Burmese pythons in Florida and the United States. Both Eutrombicula splendens (Ewing) and Eutrombicula cinnabaris (Ewing) [as E. alfreddugesi (Ouedemans)] are native and widespread in the eastern United States (Jenkins 1949, Loomis 1956), including on wildlife in Florida (Forrester 1992, Cunningham et al. 2001). Reptiles are important components of the pool of natural hosts for both species (Jenkins 1949, Loomis 1956), and the exotic origins of the Burmese python would present no barrier as an acceptable host for these polyxenous chiggers.

All wildlife, including imported reptiles, are potential hosts for ectoparasites and should be treated as “biological packages” (Davidson and Nettles 1992). When exotic reptiles are imported into the United States, they very well may be infested by ectoparasites, and these ectoparasites also may be introduced. Indeed, published records (Oliver et al. 1993) document that some have even become established in the environment in Florida. We add further evidence for potential occurrence of this phenomenon. Furthermore, several studies (Stephen and Rao 1979, Burridge et al. 2000b, Kenny et al. 2004, Reeves et al. 2006) have shown potential disease agents in the ticks that travel internationally on reptiles, another aspect of these biological packages.

We also note that new host–parasite interactions are developing among native and exotic ectoparasites and native and exotic reptile hosts in Florida. In our limited surveys of wild-caught, free-ranging exotic reptiles in Florida, we collected ticks and mites native to North America, Latin America, and Africa from reptiles native to Asia, Africa, and Central and South America. Our sample size was too small for us to estimate prevalence, but the first reports of three ectoparasites new to the United States and five new host–parasite records from 51 individual reptiles suggests that an unappreciated diversity of exotic ectoparasites may be present on free-ranging, exotic reptiles in Florida. No doubt, some of these parasites have already colonized native reptile hosts, as well, just as endemic ectoparasites have accepted and infested the introduced reptile hosts. Introduction and establishment of exotic vertebrate ectoparasites into any new environment usually leads to increased abundance and diversity of the local parasite fauna, including potential vectors for native and exotic disease agents and also may serve in the introduction of disease agents that could impact the health of local wildlife, domestic animals, and humans.

Acknowledgments

We acknowledge the assistance of SCWDS personnel, cooperators at state and federal agencies, and wildlife rehabilitation centers in the collection of these ectoparasites and the private landowners and county, state, and federal agencies that have permitted access to personal properties. Funding for this project was provided through Cooperative Agreements 0391130808CA, 0491130808CA, 0591130808CA, 0691130808CA, 0791130808CA, 0891130808CA, and 0991130808CA, Veterinary Services, Animal and Plant Health Inspection Service, U.S. Department of Agriculture. Additional funds were provided through sponsorship from the fish and wildlife agencies of Alabama, Arkansas, Florida, Georgia, Kansas, Kentucky, Louisiana, Maryland, Mississippi, Missouri, North Carolina, Puerto Rico, South Carolina, Tennessee, Virginia, and West Virginia; through the Federal Aid to Wildlife Restoration Act (50 Stat. 917) and grant agreement 06ERAG0005, Biological Resources Division, U.S. Geological Survey, U.S. Department of the Interior; and through cooperative agreements 0396130032CA, 0496130032CA, 0596130032CA, 0696130032CA, 0796130032CA, 08596130032CA, and 0996130032CA, Veterinary Services, Animal and Plant Health Inspection Service, U.S. Department of Agriculture.