Ticks (Acari: Ixodidae) Associated with Wild Animals in the Pantanal
Region of Brazil
MARCELO DE CAMPOS PEREIRA,1MATIAS PABLO JUAN SZABO´,2
GERVASIO HENRIQUE BECHARA,2ELIANA REIKO MATUSHIMA,3
JOSE´MAURI´CIO BARBANTI DUARTE,4YIGAL RECHAV,5LAURA FIELDEN,6
AND JAMES E KEIRANS7
J. Med. Entomol. 37(6): 979Ð983 (2000)
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 rela-
tionships 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 Araga ˜o, Amblyomma
pseudoconcolor Araga ˜o, Amblyomma scalpturatum Neumann, Amblyomma nodosum Neumann, Am-
blyomma 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.
ticks, Pantanal region, wild animals
TICKS ARE AMONG the most important vectors of patho-
gens that cause diseases in humans and domestic and
wild animals. In addition to the fact that they transmit
transmission) and to their progeny (vertical transmis-
sion), 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 in-
areas. The occurrence of pathogens in new hosts in-
creases 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).
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.
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 ani-
mals are abundant in this region. A survey conducted
at a ranch in Pantanal area, Nhecola ˆndia 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. (capy-
bara), Euphractus sexcinctus seosus L. (yellow arma-
dillo), Myrmecophaga tridactyla L. (giant anteater),
and Mazama gouazoubira Fisher (brown brocket
deer) were also commonly found. During the last
wild animals in the Pantanal region.
Materials and Methods
Location and Period of Collection. Ticks were col-
lected at the Alegria Farm (19? 08? S, 56? 46? W) and
some neighboring areas in the Nhecola ˆndia region of
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
1DepartamentodeParasitologia,InstitutodeCie ˆnciasBiome ´dicas,
Universidade de Sa ˜o Paulo, Av. Prof. Lineu Prestes 1374, Sa ˜o Paulo-
2Departamento de Patologia Veterina ´ria, Faculdade de Cie ˆncias
Agra ´rias e Veterina ´rias, Universidade Estadual Paulista, Jaboticabal,
SP, CEP-14870-000, Brazil.
3Departamento de Patologia, Faculdade de Medicina Veterina ´ria
e Zootecnia, Universidade de Sa ˜o Paulo, Av. Prof. Orlando Marques
de Paiva 87, Sa ˜o Paulo, S, CEP-05508-900, Brazil.
Cie ˆncias Agra ´rias e Veterina ´rias, Universidade Estadual Paulista, Ja-
boticabal, SP, CEP-14870-000, Brazil.
5Division of Viral and Rickettsial Diseases, Centers for Disease
Control and Prevention, 1600 Clifton Road, Atlanta, GA 30333.
6Science Division, Truman State University, Kirksville, MO 63501.
7Institute of Arthropodology and Parasitology, Georgia Southern
University, Statesboro, GA 30460.
0022-2585/00/0979Ð0983$02.00/0 ? 2000 Entomological Society of America
the Pantanal during three 1-wk expeditions in Sep-
tember 1996, August 1997, and April 1998. The Pan-
tanal region is drained to the west by tributaries of
the western border of the Pantanal. The land is ßat
with a slope of ?6Ð12 cm/km?1east-west and 1Ð2
and humid, whereas winter (April to September) is
warm with an average temperature of 22.1?C and dry
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 capa ˜o or cordilheira), sea-
sonally ßooded grasslands (campos), and permanent
or temporary lagoons (baõ ´as) (Alho et al. 1988). For-
dra sp., Pterocarpus rohrii Vahl, Attalea palms, Caesal-
Acosmium cardenasii Irwin & Arroyo (Schaller 1983).
patches of bromeliads and Bactris palm (Schaller
Capture of Wild Animals. Wild animals were lo-
cated visually and captured either manually with the
net system as described by Nunes et al. (1997). En-
trapment 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 collec-
tion of biological parameters were completed, sample
animals were treated for any wounds or lesions, and
released. The animals were released only after total
Tick Sample Collection. Ten to 20 min were al-
lowed for tick collection as other biological parame-
ters were collected simultaneously. Ticks from anes-
were collected with the aid of Þne forceps and stored
identiÞcation and infestation density on each animal
was evaluated in the Þrst two expeditions, and during
the third expedition only tick samples for identiÞca-
tion were collected. Tick density was presented in
three categories. Samples of free-living ticks from for-
ests (capa ˜o) 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.
A total of 81 wild animals was captured, represent-
ing 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 ani-
mals in the Pantanal. The host species captured, their
habitats, relationship between tick-infested and non-
infested animals, tick identiÞcation, and infestation
assessment are listed in Table 1. Only one tick spe-
ciesÑAmblyomma 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. ca-
jennense, 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,
entire host body. On marsh and brown brocket deer
the ticks were concentrated mainly on the neck, ster-
ticks were found attached to ventral region, ears, and
in clusters on the nipples.
25 nymphs; uncountable nymphs; seven nymphs;
two A. parvum adults; uncountable larvae; eleven
nymphs; three nymphs and one A. parvum; one
in the corresponding grassland areas.
As observed, the Pantanal region contains a wide
variety of animals and an abundance in tick species.
Results must be analyzed with caution, however, be-
cause observations were restricted to short periods of
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 micro-
habitat that prevented desiccation during the dry sea-
ticks on pampas deer during the observed period
might be explained by the fact that they live exclu-
sively in grasslands. Another interesting point was the
predominance of the nymphal stage during August
and September in the Pantanal that was similar to
the end of winter and early spring has been described
previously in South America (Guglielmone et al.
980JOURNAL OF MEDICAL ENTOMOLOGY
Vol. 37, no. 6
1990). However, more research is needed to Þnd the
seasonal activity of the ticks and the hosts that asso-
ciated 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 spe-
cies and was present on many host animals. This spe-
cies 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 (Wol-
bach), 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
inally an ectoparasite from Artiodactyla in Southeast
Asia (Tatchell 1987), was probably introduced to the
Pantanal on imported cattle and adapted to the local
Amblyomma parvum was found on brown brocket
infest a wide variety of hosts. Amblyomma tigrinum
Koch, once misidentiÞed as A. maculatum by Araga ˜o
and Fonseca (1961), was previously recorded on
M.P.J.S., and J.M.B.D. (unpublished data) but not on
coatis. A. ovale Koch was previously collected from
Pantanal region of Brazil
Captured wild hosts, habitat, relation of tick-infested/non-infested hosts, tick species found and infestation levels in the
ScientiÞc name and Common nameSubhabitat
no. of animals
Blastocerus dichotomus Illiger
Marsh1/0 B. microplus
Cervo-do Pantanal (Marsh Deer)
Veado catingueiro (brown brocket deer)
Veado campeiro (pampas deer)
Tayassu tajacu L.
Grassland 3/4B. microplus3ÑÑ
Forest/grassland1/0 Amblyomma sp.
Cateto (collared peccary)
Porco monteiro (feral pig)
(Procyonidae, Carnõ ´vora)
Quati (South American coati)
Forest/grassland 1/0Amblyomma sp.
Euphractus sexcinctus seosus
(Dasypodidae, Edentata) Tatupeba
Dasypus novemcinctus L.
Tatu-galinha (nine-banded armadillo)
Forest/grassland1/0 Amglyomma sp.
Tamandua-bandeira (giant anteater)
Tamandua tetradactyla Allen
Tamandua-mirim (collared anteater)
Caiman crocodilus yacare L.
jacare ´ (caiman)
Eunectes murinus L.
Tick infestation density was not assessed in 10 coatis from the last expedition (April 1998).
November 2000CAMPOS PEREIRA ET AL.: TICKS ASSOCIATED WITH ANIMALS IN BRAZIL
many Brazilian carnivores, including coati, anteaters,
and various rodents (Araga ˜o and Fonseca 1961). Al-
though the tick has not been described as a vector of
microorganisms infecting humans, rickettsia-like mi-
croorganisms 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 com-
mon species (Araga ˜o 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 Araga ˜o (1936), this tick is only as-
sociated with anteater species in Brazil. We collected
low armadillo. This tick was originally described from
armadillo (Dasypus sp.) and, according to Araga ˜o
(1936), immature stages also can be found on wild
birds. According to Botelho et al. (1990), Dasypodini
color. These authors also recorded A. pseudoconcolor
on yellow armadillo.
Host speciÞcity is an important issue because it
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. tigri-
num found associated with marsh deer, on three dif-
ferent 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
to pheromones that had been secreted by the males,
hebraeum Koch by Rechav et al. (1976).
of the tick-host relationships of the Pantanal region,
however much remains for investigation. The Pan-
tanal ecosystem with the habitat diversity can be con-
sidered an excellent place to investigate the relative
under ßooding conditions is another issue that should
be addressed in the Pantanal, and additional knowl-
edge undoubtedly will contribute to a better under-
standing of host-tick relationships.
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
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Received for publication 24 January 2000; accepted 16 Au-
November 2000CAMPOS PEREIRA ET AL.: TICKS ASSOCIATED WITH ANIMALS IN BRAZIL