BIOLOGY AND ECOLOGY OF AMBLYOMMA VARIEGATUM (ACARI: IXODIDAE) IN THE CARIBBEAN: IMPLICATIONS FOR A REGIONAL ERADICATION PROGRAM'

BIOLOGY AND ECOLOGY OF AMBLYOMMA VARIEGATUM (ACARI: IXODIDAE) IN THE CARIBBEAN: IMPLICATIONS FOR A REGIONAL ERADICATION PROGRAM' Nicolas Barre% and Glen I. Garris 3 (Accepted for publication 6 July 1989) ABSTRACT The concept of eradication represents a unique nlternative to the continual control of livestock ectoparasites, especially when economic losses due to the parasite orc compounded by the transmission of diseases. A successful eradicntion program depends on detailed knowledge of the biology and ecology of the targeted ectoparasite. Without I,his information, weak points in the life cycle cannot be detcnnined and exploited. We present. in this paper a review of the biology and ecoid,,'y of Amblyomma uan"ega(u/1l. (Fabricius), 8 vector of heartwater in the Caribbean, and discuss the implicatiotl.'1 of this infonnation for development or a regional eradication program. I(ey Words: Review, regional eradication program, international cooperat,ion, heartwater disease. J. Agric. Entorno!. 7(1): 1-9 (January 1990) The tropical bont tick, Amblyomma uariegatum (Fabricius), is a three host tick of African origin imported into the Caribbean region about 1830 on cattle shipped from Senegal to Guadeloupe (Currasson 1941). Heartwater, a rickettsial disease of ruminant animals caused by Cowdria ruminantium, is transmitted by A. uariegatum and is endemic on the islands of Antigua, Marie Galante, and Guadeloupe (perreau et al. 1980, Vilenberg et al. 1984, Birnie et al. 1985). Mortality in creole cattle (Bas indicus) to heartwater is less than one percent annually in Guadeloupe; however, mortality is 10 percent or more in local breeds of goats (Anonymous 1986). Furthermore, when exotic (Bas taurus) breeds of cattle or goats are imported into heartwater endemic Breas, mortality in these animals may exceed 50 percent (Callow 1978). Epidemics of dermatophilosis, an acute skin disease caused by the bacterium, Dermatophilus congolensis, usually occur soon after the arrival of A. uariegatum. The role of A. uariegatum in the epidemiology of acute dermatophilosis is unclear, but it is evident that most cattle in the Caribbean are highly susceptible to this disease. Mortality of 80 percent or more has been reported for susceptible cattle on Puerto Rico (Thoen et a1. 1980), Antigua, Martinique, St. Martin, St. Lucia, and Nevis (Uilenberg et 01. 1984). On Guadeloupe however, local B. indicus cattle and local breeds of goats are almost resistant to the disease. But when cattle are imported into Guadeloupe, this disease can cause mortality of both B. taurns and B. illdicus breeds. Presented at the Expert Consultation on Erndicntion of TickR with Special Reference to thc Americas find Caribbcun, FAD of the Unitcr! Nutions, Mexico City, Mexico, June 1987. 2 lmtitut D'Ele\lllge et de Medecine Veterinnire des PaYJI Tropicaux, C.R.A.A.G.. B. P. 1232. 97184, Poillte-a-Pitre. Cedel(, GUlldeloupe. French Wes1 Indies. United Statcs Department of Agriculture, Agriculture Research SelVice. Knipling-Rushlund U.S. Li\lcstock Insccts RClIcnrch Laborutory, P.O. Box 232, Kenville. Tcxnll 78029-0232.

2 J. Agric. Entomol. Vol. 7, No. 1 (1990) Since 1948, A. uariegatum has migrated from Guadeloupe, Marie Galante, and Antigua to at least 17 of the 35 islands of lhe Lesser Antillies and to Puerto Rico (Fig. 1). There will always be a threat of immigration of the tick and its associated diseases, heartwater. and especially dennatophilosis, as long as there are established tick populations in the Caribbean (Barre et al. 1987). It is estimated that at least one island will become infested with A. uanoegatum each year (Alderink and McCauley 1988). The recent reintroduction of A. uariegatum in St. Croix, U.S. Virgin Islands, in July 1987, after it had been eradicated in 1970 (Graham and Hourrigan 1977), and the subsequent economic losses due to dermatophilosis in a dairy herd, emphasize this point. Concern among governments and other interested organizations has prompted much debate and as a result, a regional eradication program has been proposed (Anonymous 1986, 1987). To establish appropriate eradication strategies based on application of acaricides to hosts, basic knowledge describing the life history of A. uariegatum is essential (Bram 1975, Graham J975). We present in this paper a review of the available information on the biology, ecology and survivorship both on and off the host of A. uariegatum in the Caribbean. The importance of this infolmation to the development and implementation of a regional eradication program is emphasized and discussed in light of ty,'o eradication strategies. BIOLOGY AND ECOLOGY Feeding pen'od of adults and acaricide treatment periods. Acaricide treatment intervals must coincide with the length of the feeding period of the female tick. Each subsequent treatment must be applied before the female mates, completes the engorgement process, and detaches from its host. In Africa (Rechav et al. 1982) female A. uariegatum do not attach to hosts unless there are attached males present. On Puerto Rico, females did attach to goats in the absence of males and the timing of male feeding resulted in changes in the length of the female engorgement period. When males and females were placed on goats at the same time, engorgement of mated females ranged from 11 to 16 days. If males placed in cells on goats were allowed to feed for 10 days or more before females were introduced into the cells, females engorged in a minimum of 8 days (Garris 1984, G.LG., unpublished data). Experiments conducted in Guadeloupe with adult ticks placed on goats have shown that males must be attached for at least 3 days before females will attach (N. 8., unpublished data). In other experiments, if males are attached and sexually receptive, newly introduced females will readily attach, feed, and detach in a minimum of 7 days and on the average, in 10.6 days (N.B., unpublished data). Acaricide applied to the host animal at intervals within the minimum engorgement period for adult ticks would ensure exposure of the female. The resultant control would depend on the efficacy of the acaricide used. For A. uariegatum on Guadeloupe, a lo day treatment interval (7 + 3 = 10) should be established. On Puerto Rico, the engorgement period for female ticks averaged l3.5 days in the laboratory (Garris 1984). This observation was incorporated into a successful erndication program against A. uariegatum where a treatment intelval of 14 days was used (Garris 1987, Garris et al. 1989).

BARRE und GARRIS; Eradication or A. variegalum 3 Anegd da (uleur.. CO\) 19&'1 TonoJa.. ft\~... J "0 _VIrQln Gorda }:.::.:.:~ '"p...~o~st John tdf' An9u i 11 <l ~;~~);-~ St Thom"s <1 St Hart in/st Harteen 19J8 (';:'\';'..-~-...0"'" VieQues 1981 o St hrlhe1c"'y IS><>- Solbol 1:> 5t f.us1:ll Pucr t n ic>u~ C)8",bud<l II ico St (rou St KitU, 191~ 1961 19J8 Neyhr ~ 19th century 1981 19J1.. Montserrat 198] uade v e \8]0,..IO~sirade 1982 ~_IMar; e Ga hntellb)o les Saintes 00 ~Oominica 198) A. \/4rieq4tum ~H4rtiniQUe 1948 0 Absent reported, nol established is'j ~ St lucia 19JO restricted ;n d I'Olri but ton ~-::J wide\pre4<l Vincent 1974 ap~,..oximale date of Barbado\ introduction.' 198] o heulloldtcr' prescnt: ~ 100 1,. Fig. I. A map of the Calibbean region showing the distribution of A. uan'egatum and the disease, helll'twater. The tick is found on at least 17 islands in the Caribbean. Heartwater is endemic on only three of those islands.

4 J. Agric. Entomol. Vol. 7, No. 1 (1990) Distribution of adult ticks OIl the host: special acaricide application consideration. On Guadeloupe, eleven tick-infested cattle were anesthetized, and all ticka attached were grouped according to the area of the body found and then counted. Most ticks were found on the lower extremities; l6.5% of all ticks were found attached on the dewlap, 25% in the axillary areas, 13.6% in the mammary gland - scrotal areas, and 24% in the perineum (includes the vulva and anal areas). On goats, adult ticks are frequently found attached between the digits of the feel. No adults were found attached to sides or back of goats and only four males and two females were found attached to one animal's ears. Surveys conducted in Africa have shown the same preference of attachment sites (Yeoman & Walker 1967, MacLeod et a1. 1977). The affinity of A. uariegatwn for protected areas on the body of the host requires special care in the application of aearicides. In an eradication program where hosts are sprayed with a non-systemic acaricide, considerable effort by the applicator must be given to treat those areas of the host body where ticks are found. Hosts used by A. uariegatum. 1'0 succeed in eradication, all potential hosts of the adult stages of the tick must be treated. Secondary hosts may represent reservoirs of ticks and may hamper the eradication process. For example, on St. Croix, deer were responsible for preventing the successful completion of eradication programs against Boophilus microplus (Canestrini) (Graham & Hourrigan 1977). The hosts of A. uan'egalum in Guadeloupe have been identified (Barre et al. t988). Five percent of all nymphs and 3% of all larvae found infesting the animals surveyed fed on wild animals (Table t). [n their survey, no adult A. uariegatum were found on dogs, but of 56 dogs examined by local veterinarians, six were infested with adult ticks and three of these had females atwched. The preference of adult A. uariegatum fol' large animals, und the high percentage of immature ticks found on domestic livestock in Guadeloupe (Table 1) is consistent with A. uariegatum in Africa (MacLeod 1970, Morcl 1980) llnd in Puerto Rico (Garris 1987). The knowledge that few immature ticks parasitize wild or feral animals and that larger domestic animals are preferred hosts fol' adults, favors an el'adication approach. This knowledge conbibuted to the successful eradication of.4. uanegatum from Puerto Rico (Garris et al. 1989). Because mongooses and birds are infested with some A. variegatum immatures (Barre et al. 1988), the movement of these hosts increases the risk of tick emigration from an infested area to an area where an eradication I>rogram has eliminated the tick. In an eradication progrllm, only those ticks on t.reated hosts would be exposed to acaricides. Wild secondary hosts may then temporarily isolate A. uan'egatum in marginal habitats away from exposw'e to aearicides. But since A. uariegatum adult ticks prefer to feed on domestic cattle, treatment of the domestic host will result in eradication (Garris et 81. 1989). Secondary host reinfestation problems were addressed in Puerto Rico by simultaneously treating large blocks of adjacent herds of cattle and releasing them at the same time (Gllrris et a!. 1989). A similar approach may be successful on other A. uariegatum-infested islands. Geographical distribution of A. uariegat.um on some islands in the Caribbean.. In Guadeloupe, the majority of livestock are produced in dry pasture habitats along the shore to well-drained sloping pastures below about 200 m on the mountains. 111is area averages between 1000 2800 mm of rainfau annually and has temperatures

BA RRE and GARRIS: Eradication of A. uariegatum 5 Table I. The role of secondary hosts in the life cycle of Amblyomma uanegalum (Fabricius) in Guadeloupe.* Percentage of total Percentage of total Ticks on wild animals on domestic animals Adults o 100 Nymphs 3.3 96.6 Larvae 5.1 94.9 *' Adopled from Barre el al. 1988. ranging from 22 to 25 C. All stages of A. uariegatum have been collected from domestic livestock throughout Guadeloupe year.round in these environments except in pastures higher than 200 m. In these high elevation pastures, where temperatures fall below 22 C and rainfall ranges between 1000 8000 mm annually, A uanegalum is not found attached to cattle during the cooler, wet months of the year. [n laboratory studies on Guadeloupe, A. uariegatum can complete its life cycle in a minimum of 132 days (N. 8., unpublished data) and on Puerto Rico in 142 days (Ganis 1984). Apparently in suitable habitat and climate in the Caribbean, there can be at least two generations per year (N. B., unpublished dalal, Garris 1987). In 1975, A. uariegatum was found infesting cattle in 23 herds in the central mountain region of Puerto Rico near Cidra and Cayey. By 1985, 188 farms on Puerto Rico and surrounding islands were found infested with A. [;ariegalum (Garris et al. 1989). Although environmental conditions throughout Puerto Rico were suitable for A. uariegatum sulvival, the rate of spread of this tick on the main island was slow when compared to B. microplus (Alderink and McCauley 1989). Survival of A. uariegalum off the host.. A long-teml research project to detelmine t.he maximum longevity of all stages of A. (..'Qriegatum off the hosts has been completed on Guadeloupe (N. Barrc, G. I. Garris, & R. Bonhomme, unpublished data). fn each of two different climatic zones, one urea with 1200 mm rainfall, and one area with 2800 mm rainfall per year, all sulges of A. uariegatwn were released in plastic containers covered with nylon mesh cloth. Ticks were released four times pel' year from December 1983 until March 1987 at two locations in each climatic zone; one in open pasture and one in a wooded area (shade) bordering the pasture. Among eleven releases in both low and high rainfall climatic zones, the maximum longevity was as follows: oviposition and egg incubation were completed in a maximum of 1.5 months. Larvae swvived up to 9.5 months; nymphs and flat adults survived 15 and 20 months, respectively (N. Barre, G. I. Garris, & R. Bonhomme. unpublished data). Environmental conditions in open pastures were less favorable for suivivol than those found in wooded areas. Eradication stralegies. In an eradication program based only on acaricide applications to domestic hosts, there are m'o possible ways to establish the duration of treatment. One method involves treatment of all potential hosts for maximum pelied of survivorship of the target ectoparasite (Fig. 2). For A. uan egalum on Guadeloupe. this period of time would be 46 months (l.5 + 9.5 + 15 + 20 = 46, Fig. 2). Vacated pastures become an important issue in this approach to eradication If all hosts are removed and kept from a given area for less than the 46 months required for the natural death of the ticks present when the pasture was vacated, animals upon return may become infested with ticks that have sulvived.

6 J. Agric. EntomoJ. Vol. 7, No.1 (1990) II IGil OEIISIIY or 1I0STS ON 1I0MOGENEDUS PASIURES JIl'~ATURES MAY reed ONI U1HREATED WILD AIIIMA~ ~~ LOW OENSIIY or HOSIS AIID/OR PRESENCE OF SHELTERED 10NES FOR TICKS SOI~E LARVAE FEED ON WILD HOSTS JUSI BEFORE TilE IR IIATURAL DEA 111 I J I HOIITIIS I J Max. survival of larvae SOME OF JljE RESULT WG NYMPHS FEED 011 WILD HOSIS JUSI BEFORE THEIR HAT. DEATH 115 MOtlTllS I Max. survival of nymphs ~, SOME OF IIIE RESULT WG ADULTS FEED 011 OOMEST IC 1l0STS JUST BEFORE TIIElR NATURAL DEATH Max. survival of adulls KINEr IC or CLEA/IlIIG vnries FIIOH FEW weeks 10 rew lion IllS OEPENOIIIG au TH( HELATlVE ABUNDANCE OF IRE"'fO AIll} UNTREATED HOSTS PAS lure CLEAN IN Fig. 2. An eradication strategy based on a model of the life cycle of A. variegalum in Guadeloupe based on the maximum period of survival for all stages. Another approach relies on the ability of the acaricide treatment host to collect and concentrate ticks. This method requires information on host finding rates and will depend on the parasite's host specificity. Since domestic livestock are the primary hosts for A. variegatum in the Caribbean (Garris 1987, Barre et al. 1988), this strategy could reduce the duration of an eradication program from 46 months to about 20 months (Fig. 3). A strategy of this type was successful on Puerto Rico

BARRE and GARRIS: Eradication of A. uan'egatum kc HIGH OENSITY OF HOSTS ON HOHOGEIlEOUS PASTURE ALL STAGES FEED Oil OOHESTIC TREATEO AllIHALS LOW OENSITY OF HOSTS AND/OR PRESENCE OF SHELTEREO lolie FOR ITCKS 1, J HIGH HOST FltlOltlG LOW HOST FIIIO!IIG RATE RATE (85 X/WEEK WITIl 4 ea1tui/ia) TICKS RAPIDLY EXTIRPATEO BY "TRAPPIIIG HOSTS" PASTURE CLEAN 1 TTCKS SLOWLY EXTIRPATED BY "TRAPPIIIG HOSTS HOST OTEO OF STARVATIDN,"FEWwfool-<E------ 111--------'>>-1 10 HOIHHS I <98 : ticks removcd (Hax. survival of adults) In '2 wceks with ij cattle/hal t Fig. 3. An eradication strategy based on a model of the life cycle of A. variegatum in Guadeloupe as affected by host finding rates and control with ncaricides applied to domestic livestock. when domestic livestock and dogs were treated with an acaricide for 18 months (Garris et al. 1989). Observations on the infestation rates of secondary hosts such as dogs, mongooses, and birds become an important issue in this approach to eradication. On Puerto Rico, an additional 6 month surveillance program was followed after stoppage of acaricide treatments (Garris et al. 1989). CONCLUSION From the data presented in this paper on the biology and ecology of A. vanoegatum, it is reasonable to assume that if all livestock and dogs are treated

8 J. Agric. EntomoL Vol. 7, No.1 (1990) systematically with a suitable acaricide over 8 given time period (Figures 2 and 3), the eradication of A. uariegalum from the Caribbean is possible. Obviously, each island infested with A. uariegatum presents a different challenge and thus, requires 8 different approach to eradication. Further research is needed to develop infonnation on effectiveness of new and more economical acaricides and application techniques, and on the application of these to the unique conditions which exist on each island. In this paper, we have not addressed the most important questions that will ensure success of an eradication program. Those questions involve the perception of the need for a program by the livestock producers and consumers in the Caribbean region. It will be difficult and cosuy to develop the needed producer support but without that support, it will be impossible to gather 100% of the domestic hosts of A. uariegatum for treatment with acaricides. REFERENCES CITED Alderink, F. J., and E. H. McCauley. 1988. The probabilit.y of tbe spread of Amblyomma variegatum in the Caribbean. Prevo Vet. Med. 6: 285-294. Anonymous. 1986. Management of the tropical bont tick (Amblyomma uariegatum) and associated diseases in the Caribbean - a feasibiliq' proposal Mimeograph report. December 17, 1986. Washington, DC. 105 pp. Anonymous. 1987. Report of the technical workshop on the tropical bont tick, Amblyomma uariegalum. Mimeograph report. 17-19 March 1987. Barbados, West Indies. 21 pp. Barre, N., G. Uilenberg, P. C. Morel, and E. Camus. 1987. Danger of introducing heartwater onto the American mainland: potential role of indigenous and exotic Amblyomma ticks. Ondersteport. J. Vet. Res. 54: 405-417. Barre, N., G. I. Garris, G. Borcl, and E. Camus. 1988. Hosts and population dynamics of Amblyomma uariegalum (Ac8li: Ixodidae) on Guadeloupe, French West Indies. J. Med. Entomol. 2S: 111 115. Birnie, E. r., M. J. Burridge, 8. Camus, and N. Barre. 1985. Henrlwawr in the Caribbean: isolation of Cowdria rum;mwtium from Anl.igun. Vet. Rec. 115: 121-123. Bram, R. A. 1975. Tick-borne livestock diseases and their vectors. J. The global problem. World Animal Rev. 16: 1 5. Callow, L. L. 1978. Ticks and tick-borne diseases as a barrier to the introduction of exotic cattle to the tropics. World Animal Rev. 28: 20-25. Currasson, G. 1941. Traite de protozoologie veterinaire et comparee Tome I. Tryponsomes. p. 272. Paris: Vigot. Feres Editeurs. Garris, G. I. 1984. Colonization and life cycle of Amblyomma uariecfltum (Acari: Ixodidae) in the laboratory in Puerto Rico. J. Med. Entomol. 21: 86-90. Garris, G. t. 1987. AmlJlyomma uariegatum (Acati: Ixodidae): population dynamics and hosts used during an eradication program in Puert.o Rico. J. Med. Entomol. 24: 82-86. Garris, G. I., B. H. Bokma, R. J<. StrickJand, and G. P. Combs. 1989. An evaluation of the eradication program for Amblyomma uan'cgatum (Acari: Ixodidac) on Puerto Rico. Exp. & Appl. ACMo!. 6: 67-i6. Garris, G. I., and K. Scotland. 1985. Ticks on livestock in St. Lucia. Vel. Parasitol. 18: 367 373. Graham, O. H. 1975. Planning rcsearch support for tick control programs. Proceedings of the Workshop on Ecology and Control of Ectoparasites of Cattle of Economic Importance in Latin America. 25-30 August 1975. CIAT, Cali, Columbia. 6 I>P. Graham, O. H., and J. L. Hourrigan. 1977. Eradication programs for the arthropod parasites of livestock. J. Med. Entomol. 13: 629 658.

BARRE and GARRIS: Eradication of A. variegal,um 9 MacLeod, J. 1970. Tick infestation patterns in the Southern province of Zambia. Bull. Entomol. Res. GO: 253 27.1. MacLeod, J., M. H. Colbo, M. H. Madbouly. and B. Mwanaumo. 1977. Ecological studies of ixodid ticks (Acari: Ixodidae) in Zambia. HI. Seasonal activity nnd attachment sites on cattle, with notes on other hosts. Bull. Entomo!. Res. 67: 161-173. Morel, P. C. 1980. Study on Ethiopian ticks (Acarida, lxodida). Mimeograph report. Ministry of Foreign Affairs, France, lnstitut D'Ele'lage et de Medecine Veterinairc des Pays Tropicaux. 332 ppp. Perreau, P., P. C. Morel, N. Barre, and P. Durand. 1980. Existence de la cowdriose (Heartwater) a Cowdria ruminantium chez les ruminants des Antilles frnncaises (La Guadeloupe) et des Mascareignes (La Reunion et lie J\ 1aurice). Rev. d'elevage et de Medecine Vet.erinaire des Pays Tropicaux 33: 21-22. Recha\', Y., R. A. I. Norval, and J. H. Oliver, Jr. 1982. Interspecific mating of Amblyomma hebraeum and Amblyomma uariegatum (Acari: Ixodidae). J. Med. Entomol. 19: 139 142. Thoen. C. 0., J. L. Jarnagin, D. A. Saari, B. Ortiz, and R. Harrington, Jr. 1980. Pathogenicity and trnnsmission of Demmtophilus congolensis isolated from cattle in Puerto Rico, pp. 232-237. In: Proceedings of the 84th Annual Meeting of the United States Animal Health Association. Louisville, KY 1979. Uilenberg, G., N. Barre, E. Camus, 1\'1. J. Burridge. and G. 1. Garris. 1984. Heartwater in the Caribbean, pp. 255 267. In H. P. Riemann, and M. J. Burridge, Icds], Impact or diseases on livestock production in lhe tropics. 632 pp. Yeoman. G. H., and J. B. Walker 1967. The Ixodid ticks of Tanzania. Commonwenlth Institute of Entomology, London, 358 pp.