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Ticks (Acari: Ixodidae) Associated with Wild Animals in the Pantanal Region of Brazil ´ ,2 MARCELO DE CAMPOS PEREIRA,1 MATIAS PABLO JUAN SZABO 2 GERVASIO HENRIQUE BECHARA, ELIANA REIKO MATUSHIMA,3 JOSE´ MAURIĆIO BARBANTI DUARTE,4 YIGAL RECHAV,5 LAURA FIELDEN,6 7 AND JAMES E KEIRANS

J. Med. Entomol. 37(6): 979Ð983 (2000)

ABSTRACT This paper describes the identiÞcation of ticks from wild animals of the Pantanal region in Brazil as part of a comprehensive study about established and emerging tick-host relationships and related pathological aspects. Eighty-one animals were captured (representing 13 species, six orders), and ticks were found on 63 (78%). Tick species identiÞed included Boophilus microplus (Canestrini), Amblyomma cajennense (F.), Amblyomma parvum Aragaõ, Amblyomma pseudoconcolor Aragaõ, Amblyomma scalpturatum Neumann, Amblyomma nodosum Neumann, Amblyomma ovale Koch, and Amblyomma tigrinum Koch. Dragging from grasslands yielded negative results compared with the high concentration of ticks that were collected from leaves in the forests. KEY WORDS ticks, Pantanal region, wild animals

TICKS ARE AMONG the most important vectors of pathogens that cause diseases in humans and domestic and wild animals. In addition to the fact that they transmit disease-causing agents, both to their hosts (horizontal transmission) and to their progeny (vertical transmission), the global cost of controlling ticks is estimated in millions of dollars (Sonenshine 1991). An increase in interactions among wild hosts, domestic animals, and humans may lead to the emergence of new infectious diseases or to dispersal of pathogens into new areas. The occurrence of pathogens in new hosts increases the risk of unexpected infections that result from new tick-host relationships. Animal diseases in general, and tick-borne diseases in particular plus the direct losses caused by tick attack, are among the major factors that hamper the growth of the livestock industry in developing countries (Castro 1997). Animal capture as described was submitted to and authorized by National Institute of Environment and Natural Resources of Brazil (IBAMA- Instituto Brasileiro do Meio Ambiente e dos Recursos Renova´veis). 1 Departamento de Parasitologia, Instituto de Cieˆ ncias Biome´ dicas, Universidade de Saõ Paulo, Av. Prof. Lineu Prestes 1374, Saõ PauloSP-CEP-05508-900, Brazil. 2 Departamento de Patologia Veterina´ria, Faculdade de Cieˆ ncias Agra´rias e Veterina´rias, Universidade Estadual Paulista, Jaboticabal, SP, CEP-14870-000, Brazil. 3 Departamento de Patologia, Faculdade de Medicina Veterina´ria e Zootecnia, Universidade de Saõ Paulo, Av. Prof. Orlando Marques de Paiva 87, Saõ Paulo, S, CEP-05508-900, Brazil. 4 Departamento de Melhoramento Gene´ tico Animal, Faculdade de Cieˆ ncias Agra´rias e Veterina´rias, Universidade Estadual Paulista, Jaboticabal, SP, CEP-14870-000, Brazil. 5 Division of Viral and Rickettsial Diseases, Centers for Disease Control and Prevention, 1600 Clifton Road, Atlanta, GA 30333. 6 Science Division, Truman State University, Kirksville, MO 63501. 7 Institute of Arthropodology and Parasitology, Georgia Southern University, Statesboro, GA 30460.

Many species of wild animals are common in various regions in the developing countries of the world. Large areas of South America and Africa have not been studied and little is known about ticks that are associated with wild animals as well as the disease causing agents that they transfer among hosts. One of these areas is exempliÞed by the Pantanal, a huge wet-land habitat situated east of the Paraguai River in the central region of South America. The Pantanal region is 140,000 km2 located near the western part of central Brazil at 100 m elevation and is ßooded annually between January and July. The fauna of the Pantanal is rich and numerous wild animals are abundant in this region. A survey conducted at a ranch in Pantanal area, Nhecolaˆndia subregion (Alho et al. 1988), identiÞed 34 species of mammals from seven orders, 16 families, and 28 genera. From these, Nasua nasua Tschudi (South American coati) was the most abundant animal. Other species such as Sus scrofa L. (feral pig), Ozotoceros bezoarticus L. (pampas deer), Hydrochaeris hydrochaeris L. (capybara), Euphractus sexcinctus seosus L. (yellow armadillo), Myrmecophaga tridactyla L. (giant anteater), and Mazama gouazoubira Fisher (brown brocket deer) were also commonly found. During the last century, high numbers of zebu cattle, horses, and dogs have been introduced into the area. The current paper provides information on ticks that were collected from wild animals in the Pantanal region. Materials and Methods Location and Period of Collection. Ticks were collected at the Alegria Farm (19⬚ 08⬘ S, 56⬚ 46⬘ W) and some neighboring areas in the Nhecolaˆndia region of

0022-2585/00/0979Ð0983$02.00/0 䉷 2000 Entomological Society of America

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the Pantanal during three 1-wk expeditions in September 1996, August 1997, and April 1998. The Pantanal region is drained to the west by tributaries of the Paraguay River, which then ßows southward along the western border of the Pantanal. The land is ßat with a slope of ⬇6 Ð12 cm/km⫺1 east-west and 1Ð2 cm/km⫺1 north-south (Adamoli 1982). There are two distinct seasons in the Pantanal, the summer (October to March) is hot with an average temperature of 29.1⬚C and humid, whereas winter (April to September) is warm with an average temperature of 22.1⬚C and dry (with occasional cold fronts from the south that cause abrupt decreases in air temperature). Although the Pantanal has a distinct ecosystem, it contains a few specialized habitats. The primary habitats are patches of gallery forests (called capaõ or cordilheira), seasonally ßooded grasslands (campos), and permanent or temporary lagoons (baõás) (Alho et al. 1988). Forests include trees such as Inga sp., Cecropia sp., Nectandra sp., Pterocarpus rohrii Vahl, Attalea palms, Caesalpinia floribunda Tul., Acacia paniculata Macbride, and Acosmium cardenasii Irwin & Arroyo (Schaller 1983). Coarse grass covers much of the grasslands along with patches of bromeliads and Bactris palm (Schaller 1983). Capture of Wild Animals. Wild animals were located visually and captured either manually with the aid of a lasso or a net. Deer were captured using a drive net system as described by Nunes et al. (1997). Entrapment nets 1.80 high and 100 m long were placed in a semicircle. Deer were driven into the net area by the capture team and bodily restrained. All captured animals were anesthetized with xylazine (Rompum, Bayer do Brasil S.A.) and ketamine hydrochloride (Ketalar, Park Davis do Brasil S.A). When the collection of biological parameters were completed, sample animals were treated for any wounds or lesions, and released. The animals were released only after total recovery. Tick Sample Collection. Ten to 20 min were allowed for tick collection as other biological parameters were collected simultaneously. Ticks from anesthetized wild animals and some local domestic animals were collected with the aid of Þne forceps and stored in 70⬚C ethanol until identiÞcation. Tick collection for identiÞcation and infestation density on each animal was evaluated in the Þrst two expeditions, and during the third expedition only tick samples for identiÞcation were collected. Tick density was presented in three categories. Samples of free-living ticks from forests (capaõ) and grasslands (campos) were obtained by using the dragging technique described by Rechav (1982). Drags consisted of a white ßuffy felt ßag 100 cm wide and 100 m long and attached to a handle 1 m long. Dragging was performed at no particular time of the day by pulling the drag on the forest ßoor in an area of ⬇50 m at 11 capture sites and a corresponding area at the nearest forest patch or grassland. Ticks clinging to the drag were immediately picked off with forceps and placed in 70⬚C ethanol.

Vol. 37, no. 6 Results

A total of 81 wild animals was captured, representing 13 species in six orders of which 63 (78%) were infested with ticks. Eight species of adult ticks, of which seven were from the genus Amblyomma Koch and one Boophilus Curtice, were collected from animals in the Pantanal. The host species captured, their habitats, relationship between tick-infested and noninfested animals, tick identiÞcation, and infestation assessment are listed in Table 1. Only one tick speciesÑAmblyomma cajennense (F.)Ñwas abundant on most animals. Marsh deer, brown brocket deer, coati, and giant anteater were the most infested animals, whereas pampas deer were among the less infested hosts collected. Horses and dogs carried only A. cajennense, and zebu cattle were infested mainly with Boophilus microplus (Canestrini) and A. cajennense. Ticks were removed and counted from 29 animals (second expedition). An average of 4.3 ⫾ 10.3 larvae, 37.6 ⫾ 44.6 nymphs, and 2.7 ⫾ 5.1 adult ticks per animal, respectively, were found. Ticks from highly infested animals (marsh deer, brown brocket deer, coati, and giant anteater) were seen attached over the entire host body. On marsh and brown brocket deer the ticks were concentrated mainly on the neck, sternum, and ventral region, whereas on coatis most of the ticks were found attached to ventral region, ears, and in clusters on the nipples. Dragging at 11 capture sites yielded mainly nymphs (41 nymphs and one A. cajennense adult; four nymphs; 25 nymphs; uncountable nymphs; seven nymphs; two A. parvum adults; uncountable larvae; eleven nymphs; three nymphs and one A. parvum; one nymph; two nymphs). No free-living ticks were found in the corresponding grassland areas. Discussion As observed, the Pantanal region contains a wide variety of animals and an abundance in tick species. Results must be analyzed with caution, however, because observations were restricted to short periods of the dry winter and a relatively short period of time was allowed for tick collection on each animal. The most heavily infested hosts were among those that lived in forests at the same time dragging from grasslands yielded negative results as opposed to the high concentration of ticks collected from leaves on the forest ßoor. It is probable that the leaves on the forest ßoor provided the best humidity conditions for the survival of Amblyomma ticks, providing a microhabitat that prevented desiccation during the dry season. In this regard, we speculated that low numbers of ticks on pampas deer during the observed period might be explained by the fact that they live exclusively in grasslands. Another interesting point was the predominance of the nymphal stage during August and September in the Pantanal that was similar to other reports. Nymphal activity of Amblyomma spp. at the end of winter and early spring has been described previously in South America (Guglielmone et al.

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Table 1. Captured wild hosts, habitat, relation of tick-infested/non-infested hosts, tick species found and infestation levels in the Pantanal region of Brazil

ScientiÞc name and Common name

Subhabitat

Relation of Infested/ non-infested hosts

Tick species

Infestation level/ no. of animals 1Ð10 ticks

11Ð100 ticks

⬎100 ticks

Ñ

Ñ

1

Ñ

4

3

3

Ñ

Ñ

Blastocerus dichotomus Illiger (Cervidae, Artiodactyla)

Marsh

1/0

Cervo-do Pantanal (Marsh Deer) Mazama gouazoubira (Cervidae, Artiodactyla) Veado catingueiro (brown brocket deer) Ozotoceros bezoarticus (Cervidae, Artiodactyla) Veado campeiro (pampas deer) Tayassu tajacu L.

Forest

7/0

Grassland

3/4

B. microplus

Forest/grassland

1/0

Amblyomma sp. (immatures)

Ñ

1

Ñ

Forest/grassland

1/0


1

Ñ

Ñ

Forest/grassland

38/3

10

12

6

Forest/grassland

2/5

A. cajennense A. ovale A. tigrinum A. parvum Amblyomma sp. (immatures) A. pseudoconcolor

2

Ñ

Ñ

Forest/grassland

1/0

1

Ñ

Ñ

Forest/grassland

3/0

Amglyomma sp. (immatures) A cajennense A. scalpturatum Amblyomma sp. (immatures)

Ñ

2

1

Forest/grassland

3/0

3

Ñ

Ñ

Forest/grassland/lagoon

2/3

A. cajennense A. nodosum Amblyomma sp. (immatures) A cajennense

2

Ñ

Ñ

Lagoon/marsh

0/3

None

Ñ

Ñ

Ñ

Lagoon/marsh

1/0


1

Ñ

Ñ

(Tayassuidae, Artiodactyla) Cateto (collared peccary) Sus scrofa (Artiodactyla) Porco monteiro (feral pig) Nasua nasua (Procyonidae, Carnõ´vora) Quati (South American coati)

Euphractus sexcinctus seosus (Dasypodidae, Edentata) Tatupeba (yellow armadillo) Dasypus novemcinctus L. (Dasypodidae, Edentata) Tatu-galinha (nine-banded armadillo) Myrmecophaga tridactyla (Myrmecophagidae, Edentata) Tamandua-bandeira (giant anteater) Tamandua tetradactyla Allen (Myrmecophagidae, Edentata) Tamandua-mirim (collared anteater) Hydrochaeris hydrochaeris (Hydrochaeridae, Rodentia) Capivara (Capybara) Caiman crocodilus yacare L. (Crocodilidae, Crocodilia) jacare´ (caiman) Eunectes murinus L. (Boidae, Squamata) sucuri (anaconda)

B. microplus A. cajennense A. tigrinum B. microplus A. cajennense A. parvum

Tick infestation density was not assessed in 10 coatis from the last expedition (April 1998).

1990). However, more research is needed to Þnd the seasonal activity of the ticks and the hosts that associated with them. Considering the limitations of tick collection, the main importance of the present work was to report tick species on wild animals under relatively natural conditions. A. cajennense was the most common species and was present on many host animals. This species is widely distributed in South America and its immature stages are not host speciÞc (Lopes et al. 1998). A. cajennense is described as the main vector of the spotted fever agent, Rickettsia rickettsii (Wolbach), in Latin America (Lemos et al. 1996) and is associated with horses and capybaras (Campos Pereira and Labruna 1998). The presence of B. mi-

croplus on the Brazilian deer species was previously described by Serra-Freire et al. (1996). This tick, originally an ectoparasite from Artiodactyla in Southeast Asia (Tatchell 1987), was probably introduced to the Pantanal on imported cattle and adapted to the local Artiodactyla. Amblyomma parvum was found on brown brocket deer and coatis as well as free living among leaves. Our record of this tick on coatis indicates that this tick may infest a wide variety of hosts. Amblyomma tigrinum Koch, once misidentiÞed as A. maculatum by Aragaõ and Fonseca (1961), was previously recorded on marsh deer by Serra-Freire et al.(1996) and by M.C.P, M.P.J.S., and J.M.B.D. (unpublished data) but not on coatis. A. ovale Koch was previously collected from

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many Brazilian carnivores, including coati, anteaters, and various rodents (Aragaõ and Fonseca 1961). Although the tick has not been described as a vector of microorganisms infecting humans, rickettsia-like microorganisms were isolated from one A. ovale tick in the State of Minas Gerais, Brazil (Lemos et al. 1997), and a human case of tick bite paralysis due to A. ovale was reported in Panama (Obaldia 1992). Amblyomma scalpturatum Neumann is not a common species (Aragaõ 1936) and has been associated mainly with Tapir (Tapirus terrestris L.) and rarely on anteater and dog (Jones et al. 1972). Amblyomma nodosum was found exclusively on collared anteater, and according to Aragaõ (1936), this tick is only associated with anteater species in Brazil. We collected Amblyomma pseudoconcolor Aragaõ only from the yellow armadillo. This tick was originally described from armadillo (Dasypus sp.) and, according to Aragaõ (1936), immature stages also can be found on wild birds. According to Botelho et al. (1990), Dasypodini are probably the real indigenous hosts of A. pseudoconcolor. These authors also recorded A. pseudoconcolor on yellow armadillo. Host speciÞcity is an important issue because it establishes the potential of a vector to carry pathogens between host species. According to results presented here and in previous reports, A. ovale, A. parvum, and A. cajennense seem to lack a strict host speciÞcity and are major candidates for dissemination and vectoring of infections with new pathogens. However, A. tigrinum found associated with marsh deer, on three different locations in Brazil, might indicate a natural host-parasite relationship or adaptation of this tick to the marsh environment. On coatis, the nymphs attached in clusters around the nipples. Adults of Amblyomma ticks were found on coati and we assumed that the nymphs were attracted to pheromones that had been secreted by the males, similar to the phenomenon previously described for A. hebraeum Koch by Rechav et al. (1976). The current work presents some interesting insights of the tick-host relationships of the Pantanal region, however much remains for investigation. The Pantanal ecosystem with the habitat diversity can be considered an excellent place to investigate the relative importance of environment and adaptation to hosts in the establishment of tick-host speciÞcity. Tick survival under ßooding conditions is another issue that should be addressed in the Pantanal, and additional knowledge undoubtedly will contribute to a better understanding of host-tick relationships. Acknowledgments We thank Heitor Moreira Herrera for his assistance and for putting Alegria Farm at our disposal. We are also indebted to our students who helped capture animals and turned the expedition into a joyful event (FiÞ, Paquita, Beterraba, Bira, Preta, Rita, Heitor, Hermo´ genes, and the staff of Alegria Farm). IBAMA kindly gave permission for the capture of animals. This research was supported by FAPESP, CNPq and University of Saõ Paulo.

Vol. 37, no. 6 References Cited

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Serra-Freire, N. M., M. Amorim, G. S. Gazeta, L. Guerim, and M.H.G. Deside´rio. 1996. Deer ixodofauna in Brazil. Rev. Bras. Cienc. Vet. 3: 51Ð54. Sonenshine, D. E. 1991. Biology of ticks, vol. 1. Oxford University Press, New York.

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