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Home , Flumethrin, Tick infestation

Article #3 CE Controlling and Eradicating on Reptiles

Michael J. Burridge, BVM&S, MPVM, PhD University of Florida

ABSTRACT: This article describes practical protocols for controlling and eradicating tick infestations on reptiles and their premises. Protocols for eradicating involve administering per- methrin (i.e., Provent-a-mite, Pro Products, Mahopac, NY) directly on tortoises and indi- rectly on snakes and lizards as well as concurrently treating tortoise facilities with and snake and lizard facilities with .

lthough ticks are common parasites on garine infections in boa constrictors (Boa con- wild lizards, snakes, and tortoises in the strictor), shingleback skinks (Trachydosaurus United States,1–6 previously they were rugosus), rough-tailed agamas (Laudakia stellio), A 8 seldom brought to the attention of veterinarians. and Greek tortoises (Testudo graeca). However, with the dramatic growth of interna- It was not until events that occurred in Florida tional trade in live reptiles (many of which are in the late 1990s that the need for developing safe infested with exotic ticks7–8) during the past and efficacious protocols for controlling and decade, the tick problem in reptiles became a eradicating tick infestations on reptiles became concern for veterinarians. In 1997, an estimated apparent. Following identification of an estab- 1,700,000 reptiles were imported into the lished population of exotic African tortoise ticks United States and 9,300,000 reptiles were ( marmoreum; Figure 1) on a reptile- exported.9 In 2000, an estimated 8,600,000 rep- breeding operation in central Florida in 1997,14 tiles and amphibians were kept as pets in the subsequent investigations found that at least eight United States. Despite the large numbers of pet exotic tick species were being imported into reptiles and the frequency with which they are Florida on reptiles.15 Two of these exotic species, infested with ticks, there are few published Amblyomma sparsum and A. marmoreum, were a reports of direct pathogenic effects of ticks on particular concern because both are proven exper- reptiles. Heavy infestations with the exotic tick imental vectors of Ehrlichia (Cowdria) ruminan- Amblyomma (Aponomma) exornatum in the nasal tium, the rickettsia that causes heartwater, an passages of monitor lizards can cause suffoca- acute tick-borne disease of domestic and wild tion and death,10–11 and the iguana tick Ambly- ruminants.16,17 One shipment of leopard tortoises omma dissimile has reportedly caused ulcers at (Geochelone pardalis) imported into Florida from the site of attachment on rainbow boas (Epi- Zambia in 1999 was found to be infested with A. crates cenchria).12 Another report13 suggested that sparsum, some of which tested positive for heavy tick infestations could E. ruminantium infection.18 This illustrated that Full-text articles and CE testing at significantly limit the aerobic continued international dissemination of A. spar- CompendiumVet.com. Send comments/ capacity and behavior of lizard sum on tortoises exported from Africa posed a questions via email compendium@ medimedia.com, fax 800-556-3288, hosts. In addition, ticks are real risk for the spread of heartwater to the or web CompendiumVet.com. known vectors of hemogre- United States and elsewhere.

May 2005 371 COMPENDIUM 372 CE Controlling and Eradicating Tick Infestations on Reptiles

Subsequent research at the University of Florida has defined the optimal acaricide for use on reptiles. The goal of the first phase of the study was to determine the safety and efficacy of acaricides using A. marmoreum ticks and leopard tortoises as hosts.26 Because no acaricide was reg- istered for use on reptiles in the United States, acaricides registered for use on other domestic animals were investigated, including , , , cyfluthrin, , lin- dane, permethrin, and . Only four of the acaricides (i.e., chlorpyrifos, cyfluthrin, lin- dane, permethrin) produced 100% tick mortality within 24 hours of application, and only two (i.e., cyfluthrin, permethrin) continued to cause Figure 1. African tortoise ticks (A. marmoreum; inset), including a 100% mortality when diluted as much as fully engorged female, attached to a leopard tortoise (G. pardalis). 1:10,000. Five of the acaricides (i.e., amitraz, car- baryl, chlorpyrifos, cyfluthrin, permethrin) were studied further for toxicity to leopard tortoises. These findings stimulated an interest in a safe and The results indicated that cyfluthrin and permethrin, efficacious method of controlling tick infestations on the two most effective acaricides, were also the safest. reptiles. A search of the veterinary literature found little The goal of the second phase of the study was to identify useful information on the safety and efficacy of acari- an optimal acaricide formulation for controlling ticks on cides for controlling ticks on reptiles, apparently because reptiles. Previous reports had shown that several acaricides the demand had been too small to interest manufactur- were toxic to reptiles when applied dermally or as aerosols. ers and testing of reptiles was not a requirement for pes- Toxic reactions to cyfluthrin, , flumethrin, ticide registration.19 Consequently, a research program , and pyrethrins had been seen in snakes27–31;to was initiated at the University of Florida to develop chlorpyrifos, cyfluthrin, deltamethrin, , practical protocols for controlling ticks on infested flumethrin, , , and pyrethrins in premises, and the results are summarized in this article. lizards27,32; and to ivermectin in tortoises.24 Furthermore, carbaryl and chlorpyrifos produced the unwanted side CONTROLLING TICKS ON REPTILES effect of eye irritation in tortoises.26 In contrast, permethrin There have been very few reports of acaricide admin- had been used safely on tortoises,26 snakes,27,29,30,33 and istration to treat tick infestations on reptiles. Two lizards.27 Consequently, permethrin became the acaricide of reports from South Africa discussed using acaricides to choice for tick control in reptiles. However, it was realized treat tortoises infested with A. marmoreum. The first was that different acaricide formulations contain different a retrospective report of an owner treating a pet tortoise ingredients in addition to the active compound, some of with carbaryl solution,20 and the second report summa- which might be toxic to reptiles. For example, piperonyl rized an experiment using amitraz to induce detachment butoxide, which is added to some formulations as a syner- of A. marmoreum to facilitate a tick survey.21 Neither gist, has been associated with snake mortality.28 Therefore, report scientifically evaluated either the efficacy or commercially available permethrin formulations were safety of administering acaricides to treat tick-infested examined. Only one (i.e., Provent-a-mite [Pro Products, tortoises. Two other short reports from England22 and Mahopac, NY], a patented formulation34 containing 0.5% India23 found that the endectocide ivermectin controlled permethrin) had been prepared specifically for use on rep- ticks on snakes when given subcutaneously, but iver- tiles, had received Section 18 Exempt registration from the mectin has been shown to be toxic in tortoises.24 A US Environmental Protection Agency (registration No. recent publication suggested using 0.25% fipronil to 50404-7-73617), and had been marketed in the United control ticks on reptiles with the caveat that further States for several years as an acaricide to control mites and evaluation is needed.25 ticks that feed on reptiles. The clinical effects of applying

COMPENDIUM May 2005 Controlling and Eradicating Tick Infestations on Reptiles CE 373

Protocols for Controlling Ticks In the recommended protocol for controlling ticks on reptiles, the permethrin product Provent-a-mite is used directly with tortoises and indirectly with snakes and lizards.

Large tortoises (>2 lb [0.91 kg]) • Spray two 1-sec bursts of Provent-a-mite directly into each leg opening from a distance of 12–15 inches (30–38 cm). • When spraying foreleg openings, protect the tortoise’s eyes with a barrier such as a piece of cardboard.

Small tortoises (<2 lb [0.91 kg]) A. Spraying a young African spurred tortoise (G. sulcata) • Spray one 1-sec burst of Provent-a-mite directly into with a permethrin formulation (i.e., Provent-a-mite) to each leg opening from a distance of 12–15 inches control tick . (30–38 cm; A). • When spraying foreleg openings, protect the tortoise’s eyes with a barrier such as a piece of cardboard.

Snakes and lizards • Remove snakes or lizards and their water from the container. • When the container is empty, spray the substrate with Provent-a-mite from a distance of 12–15 inches (30–38 cm) at a rate of 1 sec of spray per 1 sq ft (930 cm2; B). • Allow the acaricide to dry, and confirm that all vapors B. Spraying the substrate in a snake container with a have disappeared before returning snakes or lizards permethrin formulation (i.e., Provent-a-mite) to and their water to the container. indirectly control tick infestation.

Provent-a-mite were studied on three species of reptiles by infestations. Three species of exotic ticks recently estab- direct application to African spurred tortoises (Geochelone lished breeding colonies on at least five reptile premises sulcata) and application to the bedding of rosy boas (Licha- in Florida. They were A. marmoreum at three tortoise- nura trivirgata) and green iguanas (Iguana iguana), using breeding facilities,14,36 A. sparsum at another tortoise- 10 times the recommended dose every fifth day for a total breeding facility,36 and Amblyomma (Aponomma) of six applications.35 Despite the excessive doses of acari- komodoense in a lizard exhibit at a zoo.37 The Florida cli- cides, no evidence of toxic reactions related to the perme- mate will likely be suitable to maintain other exotic tick thrin formulation was found in any of the three species of species imported from tropical and subtropical regions reptiles treated, suggesting that Provent-a-mite is a safe of the world, with unknown consequences for native acaricide for controlling ticks on tortoises, snakes, and fauna in the absence of adequate control measures. Con- lizards (see box on this page). sequently, there was an urgent need to eradicate estab- lished exotic tick infestations to minimize the risk that ERADICATING TICK INFESTATIONS they would spread to native fauna. FROM REPTILE PREMISES Protocols for eradicating exotic tick infestations were Controlling tick infestations on reptiles is an ongoing developed at the University of Florida to minimize the activity on premises where ticks have developed breed- risk that exotic ticks would spread to native fauna and ing colonies. In these situations, tick eradication is the thus become established in the United States as had preferable goal, especially when dealing with exotic tick happened in past years in Florida with the iguana tick

May 2005 COMPENDIUM 374 CE Controlling and Eradicating Tick Infestations on Reptiles

Protocols for Eradicating Ticks The recommended protocols for eradicating tick infestations from reptile facilities depend on the type of reptile involved.

Tortoise facilities • Treat all tortoises with Provent-a-mite. • Move treated tortoises to a tick-free area. • Have the premises sprayed with a cyfluthrin product (e.g., Tempo, Bayer Corporation, Kansas City, MO) by a licensed pest-control company, ensuring that all surface areas, including housing and burrows, are treated (A). • Have the premises sprayed again 2 weeks later. A. Spraying a tortoise enclosure with a cyfluthrin • One week after the second premises treatment, place formulation to eradicate tick infestation. sentinel tortoises on the treated premises, and allow them to roam freely for 10 days. • Spray the indoor enclosure, including hide boxes, • If the sentinels remain free of ticks, eradication of the with Provent-a-mite, following the same guidelines infestation can be considered successful. as for the outdoor enclosure. • If the sentinels become infested with ticks, repeat the • After the first treatment, select two small test areas protocol until they remain free of ticks. (approximately 12 × 12 in [30 × 30 cm])—one from the indoor enclosure and the other from the outdoor Snake or lizard facilities enclosure—and spray them with Provent-a-mite. • Secure snakes or lizards in their indoor enclosure. • Place 15 sentinel house crickets (Acheta domestica) in • Spray the outdoor enclosure with Provent-a-mite at a an overturned plastic container in each test area every rate of one can (i.e., 170 g) per 25 m2 from a distance 2 weeks. of 12 inches (30 cm). Pay special attention to • If the treated test area fails to kill sentinel suspected tick-molting areas such as the base of walls, within 15 minutes, retreat the area with Provent-a- between boards, under ledges and rocks, around the mite as already described. base of basking spots, and cracks or holes. • If no ticks are found after two consecutive treatments, • Allow the acaricide to dry. eradication of the infestation can be considered • Release snakes or lizards in their outdoor enclosure. successful.

A. dissimile38 and the rotund toad tick Amblyomma rotun- was sprayed with Provent-a-mite. Once the acaricide had datum.39 The protocol adopted for tortoises required all dried, the reptiles were released from their pen area, which tortoises on infested premises be sprayed with the per- was then closed and sprayed with the same product. This methrin product Provent-a-mite followed by spraying of treatment was repeated until no further ticks were identi- the premises by a licensed pest-control company with a fied on the reptiles or their premises. With this protocol cyfluthrin product specifically formulated for premises (see box on this page), an exotic tick infestation was eradi- treatment.36 Successful eradication was determined by cated from the Komodo dragon (Varanus komodoensis) placing tick-free sentinel tortoises on the treated prem- exhibit at a zoo in Florida over a 6-month period; in the ises (the infestation was considered eradicated when the 18 months since the eradication program was terminated, sentinels remained free of ticks). With this protocol (see not a single tick has been detected in the exhibit.37 box on this page), an exotic tick infestation was eradi- cated from a tortoise facility in Florida.36 REFERENCES A different protocol was necessary for lizards and snakes 1. Bishopp FC, Trembley HL: Distribution and hosts of certain North Ameri- can ticks. J Parasitol 31:1–54, 1945. because direct application of acaricide was contraindicated 2. Wilson N, Kale WH: Ticks collected from Indian River County, Florida in them, especially in endangered and dangerous species. (Acari: Metastigmata: Ixodidae). Florida Entomol 55:53–57, 1972. 3. Apperson CS, Levine JF, Evans TL, et al: Relative utilization of reptiles and The protocol adopted for lizards and snakes required them rodents as hosts by immature scapularis (Acari: Ixodidae) in the coastal to be secured in their pens while the rest of the premises plain of North Carolina, USA. Exp Appl Acarol 17:719–731, 1993.

COMPENDIUM May 2005 Controlling and Eradicating Tick Infestations on Reptiles CE 375

4. Wright SA, Lane RS, Clover JR: Infestation of the southern alligator lizard 32. Kihara H, Yamashita H: The lethal effects of pesticides to reptiles. Snake 10: (Squamata: Anguidae) by (Acari: Ixodidae) and its susceptibil- 10–15, 93–94, 1978. ity to . J Med Entomol 35:1044–1049, 1998. 33. Zeman P, Hrebik T, Rupes V: Diffusil V: Zkusenosti s novym veterinárním 5. Schall JJ, Prendeville HR, Hanley KA: Prevalence of the tick Ixodes pacificus insekticidním prípravkem. Veterinarstri 36:565–567, 1986. on western fence lizards, Scleroporus occidentalis: Trends by gender, size, sea- 34. Pound R: Mite and tick control for reptiles. Washington, United States son, site, and mite infestation. J Herpetol 34:160–163, 2000. Patent and Trademark Office, patent no. 6,121,318. 6. Eisen RJ, Eisen L, Lane RS: Prevalence and abundance of Ixodes pacificus 35. Burridge MJ, Simmons LA, Hofer CC: Clinical study of a permethrin for- immatures (Acari: Ixodidae) infesting western fence lizards (Sceloporus occi- mulation for direct or indirect use in control of ticks on tortoises, snakes and dentalis) in northern California: Temporal trends and environmental corre- lizards. J Herpetol Med Surg 13:16–19, 2003. lates. J Parasitol 87:1301–1307, 2001. 36. Burridge MJ, Simmons LA, Peter TF, Mahan SM: Control and eradication 7. Burridge MJ: Ticks (Acari: Ixodidae) spread by the international trade in rep- of chelonian tick infestations, with particular reference to vectors of heartwa- tiles and their potential roles in dissemination of diseases. Bull Entomol Res ter. Ann N Y Acad Sci 969:294–296, 2002. 91:3–23, 2001. 37. Burridge MJ, Simmons LA, Condie T: Control of an exotic tick (Aponomma 8. Burridge MJ, Simmons LA: Exotic ticks introduced into the United States komodoense) infestation in a Komodo dragon (Varanus komodoensis) exhibit at on imported reptiles from 1962 to 2001 and their potential roles in interna- a zoo in Florida. J Zoo Wildl Med 35:248–249, 2004. tional dissemination of diseases. Vet Parasitol 113:289–320, 2003. 38. Bequaert J: Amblyomma dissimile Koch, a tick indigenous to the United States 9. Franke J, Telecky TM: Reptiles as Pets: An Examination of the Trade in Live (Acarina: Ixodidae). Psyche 32:45–47, 1932. Reptiles in the United States. Washington, The Humane Society of the United 39. Oliver JH, Hayes MP, Keirans JE, Lavender DR: Establishment of the for- States, 2001. eign parthenogenetic tick Amblyomma rotundatum (Acari: Ixodidae) in 10. Young E: Aponomma exornatum (Koch) as a cause for mortality among moni- Florida. J Parasitol 79:786–790, 1993. tors. J S Afr Vet Med Assoc 36:579, 1965. 11. Norval RAI: The ticks of Zimbabwe. XI. The genus Aponomma. Zimbabwe Vet J 16:5–8, 1985. 12. Dunn LH: Studies on the iguana tick, Amblyomma dissimile, in Panama. J ARTICLE #3 CE TEST Parasitol 5:1–10, 1918. CE 13. Dunlap KD, Mathies T: Effects of nymphal ticks and their interaction with This article qualifies for 2 contact hours of continuing malaria on the physiology of male fence lizards. Copeia 4:1045–1048, 1993. education credit from the Auburn University College of 14. Allan SA, Simmons LA, Burridge MJ: Establishment of the tortoise tick Veterinary Medicine. Subscribers may purchase individual Amblyomma marmoreum (Acari: Ixodidae) on a reptile-breeding facility in CE tests or sign up for our annual CE program. Those Florida. J Med Entomol 35:621–624, 1998. 15. Burridge MJ, Simmons LA, Allan SA: Introduction of potential heartwater who wish to apply this credit to fulfill state relicensure vectors and other exotic ticks into Florida on imported reptiles. J Parasitol 86: requirements should consult their respective state 700–704, 2000. authorities regarding the applicability of this program. 16. Norval RAI, Mackenzie PKI: The transmission of Cowdria ruminantium by Amblyomma sparsum. Vet Parasitol 8:189–191, 1981. To participate, fill out the test form inserted at the end 17. Peter TF, Burridge MJ, Mahan SM: Competence of the African tortoise tick, of this issue or take CE tests online and get real-time Amblyomma marmoreum (Acari: Ixodidae), as a vector of the agent of heart- scores at CompendiumVet.com. water (Cowdria ruminantium). J Parasitol 86:438–441, 2000. 18. Burridge MJ, Simmons LA, Simbi BH, et al: Evidence of Cowdria ruminan- tium infection (heartwater) in Amblyomma sparsum ticks found on tortoises 1. The primary reason for the increased prevalence imported into Florida. J Parasitol 86:1135–1136, 2000. 19. Hall RJ, Henry PFP: Assessing effects of pesticides on amphibians and rep- of ticks on pet reptiles in the United States is tiles: Status and needs. Herpetol J 2:65–71, 1992. a. the increased numbers of ticks on native reptiles. 20. Walker JB, Bezuidenhout JD: Treatment of tick-infested tortoises. J S Afr Vet b. the dramatic growth of international trade in live Assoc 44:381, 1973. 21. Petney TN, Knight MM: The treatment of ticks on tortoises using amitraz. J reptiles. S Afr Vet Assoc 59:206, 1988. c. global warming. 22. Lawrence K: Ivermectin as an ectoparasiticide in snakes. Vet Rec 115:441– d. the lack of effective acaricides for use on reptiles. 442, 1984. 23. Thiruthalinathan R, Pannerselvam N, Swaminathan D: Efficacy of iver- mectin against ticks on snakes. J Vet Parasitol 9:37–39, 1995. 2. How many reptiles and amphibians were esti- 24. Teare JA, Bush M: Toxicity and efficacy of ivermectin in chelonians. JAVMA mated to be kept as pets in the United States in 183:1195–1197, 1983. 25. Carpenter JW, Mashima TY, Rupiper DJ: Exotic Animal Formulary, ed 2. 2000? Philadelphia, WB Saunders, 2001. a. 600,000 c. 5,600,000 26. Burridge MJ, Peter TF, Allan SA, Mahan SM: Evaluation of safety and efficacy b. 2,600,000 d. 8,600,000 of acaricides for control of the African tortoise tick (Amblyomma marmoreum) on leopard tortoises (Geochelone pardalis). J Zoo Wildl Med 33:52–57, 2002. 27. Mutschmann F: Ektoparasitenbekämpfung bei Reptilien mit synthetischen 3. Heavy tick infestations can cause suffocation and Pyrethroiden?, in Internationales Colloquium fur Pathologie und Therapie der death in Reptilien und Amphibien. Germany, Giessen/Lahn, Deutsche Veterinarmedi- zinische Gesellschaft, 1991, pp 95–106. a. leopard tortoises. c. ball pythons. 28. Brooks JE, Savarie PJ, Bruggers RL: The toxicity of commercial b. monitor lizards. d. green iguanas. aerosol formulations to brown tree snakes. Snake 28:23–27, 1998. 29. Brooks JE, Savarie PJ, Johnston JJ, Bruggers RL: Toxicity of / pyrethoid fogger products to brown tree snakes, Boiga irregularis, in cargo 4. Ticks are known vectors of hemogregarine infec- containers. Snake 28:33–36, 1998. tions in 30. Brooks JE, Savarie PJ, Johnston JJ: The oral and dermal toxicity of selected chemicals to brown tree snakes (Boiga irregularis). Wildl Res 25:427–435, 1998. a. boa constrictors. c. Greek tortoises. 31. Messonnier S: Treat pyrethrin toxicity in snakes. Exot Pet Pract 3:20, 1998. b. rough-tailed agamas. d. all of the above

May 2005 COMPENDIUM 376

5. The endectocide ivermectin is reportedly toxic in a. snakes. c. tortoises. b. lizards. d. none of the above 6. The acaricide of choice for controlling ticks on tortoises, snakes, and lizards is a. permethrin. c. fipronil. b. amitraz. d. pyrethrins. 7. Direct application of acaricide is recommended only for a. lizards. c. turtles. b. snakes. d. tortoises. 8. The acaricide ______can be used as a safe and effective premises spray to eradicate ticks from a tortoise facility. a. amitraz c. carbaryl b. cyfluthrin d. fipronil 9. Reptilian ticks carrying exotic pathogens have been found on imported a. lizards. c. tortoises. b. snakes. d. turtles. 10. Reptilian ticks carrying exotic pathogens have been found on reptiles imported from a. Africa. c. Australia. b. Asia. d. South America.