Ticks (Acari: Ixodidae) on Wild Marsh-Deer - BioOne

POPULATION AND COMMUNITY ECOLOGY

Ticks (Acari: Ixodidae) on Wild Marsh-Deer (Blastocerus dichotomus) from Southeast Brazil: Infestations Before and After Habitat Loss ´ ,1 MARCELO B. LABRUNA,2 MARCELO C. PEREIRA,3 MATIAS P.J. SZABO JOSE´ MAURIĆIO B. DUARTE4

AND

Departamento de Patologia Veterina´ria, Faculdade de Cieˆ ncias Agra´rias e Veterina´rias, Universidade Estadual Paulista, Jaboticabal SP, Brazil; and Universidade de Franca, Franca SP, Brazil

J. Med. Entomol. 40(3): 268Ð274 (2003)

ABSTRACT The lake from Porto-Primavera hydroelectric power station inundated an area of 2,200 km2 at the border of Saõ Paulo and Mato-Grosso do Sul States, Brazil. Infestations by ticks were evaluated on 135 marsh deer, Blastocerus dichotomus (Illiger), captured before and after inundation. Ticks were collected for identiÞcation, and infestation level of animals was assessed by scoring. Deer were divided into four groups according to capture location and temporal relation to the inundation. Groups 1, 2, and 3 were captured before inundation. Group 4 was captured after inundation. Four tick species were found: Amblyomma cajennense (F.), Amblyomma triste Koch, Anocentor nitens (Neumann), and Boophilus microplus (Canestrini). Groups 1, 2, 3, and 4 had 30, 45, 100, and 96%, respectively, of animals carrying B. microplus ticks. A. triste was observed on 16, 22, 22, and 88% of animals from groups 1, 2, 3, and 4, respectively. A. nitens and A. cajennense were observed only on group 4, on 32 and 16% of the animals, respectively. Groups 1 and 2 had only 4.8 and 6.1% of animals with high infestation levels, respectively, and no ticks on 46.8% and 45.5% of the animals, respectively. Conversely, groups 3 and 4 lacked noninfested animals and had high infestation levels on 77.8 and 50% of deer, respectively. Marsh area shrinkage was blamed for higher infestation levels on deer from groups 3 and 4. The widespread presence of A. triste on marsh deer, a Neotropical tick species, raises the possibility of a natural hostÐparasite relationship. KEY WORDS marsh deer, Blastocerus dichotomus, Boophilus microplus, Amblyomma triste, Amblyomma cajennense, Anocentor nitens

THE EVER-GROWING CONCERN WITH wildlife preservation increases the need for knowledge regarding wildlife management. Such management demands knowledge about parasitism under natural conditions to permit the detection of potential threats for host species survival. Captive animals are exposed to infections and infestations associated with the new environment. Reintroduction programs and translocation of wild animals to new environment are specially a delicate matter because hostÐparasite relationships cannot be

We followed the protocol, which agrees with Ethical Principles in Animal Research adopted by the National Institute of Environment and Natural Resources of Brazil (IBAMA; Instituto Brasileiro do Meio Ambiente e dos Recursos Renova´veis). Permits and approvals are on Þle in the ofÞce of J.M.B.D. 1 E-mail: szabo@fcav.unesp.br. 2 Departamento de Medicina Veterina ´ria Preventiva e Sau´ de Animal, Faculdade de Medicina Veterina´ria e Zootecnia, Universidade de Saõ Paulo, Saõ Paulo, SP 05508-000, Brazil. 3 Departamento de Parasitologia, Instituto de Cie ˆ ncias Biome´ dicas, Universidade de Saõ Paulo, Saõ Paulo, SP 05508-900, Brazil. 4 Departamento de Melhoramento Gene ´ tico, Faculdade de Cieˆ ncias Agra´rias e Veterina´rias, Universidade Estadual Paulista, Jaboticabal, SP 14884-900, Brazil.

closely monitored in the new habitat and the introduced animals can be exposed to or spread pathogenic agents to local fauna. The outcome of such relationships is, most of the time, unpredictable. Knowledge of original parasitic fauna might help to avoid or to predict many of the undesirable consequences of reintroduction programs. In this context, determination of parasites occurring naturally in the environment and on animal species is of utter importance. Information regarding ticks on South American deer species, especially on free-living animals, is scarce in current literature, and more data are needed to guide technicians involved in the handling of such animals, freeliving or captive. Ticks are obligate ectoparasites that infest mammals, birds, reptiles, and amphibians. They rank second only to mosquitoes as arthropod vectors and surpass all others in the variety of pathogenic organisms they transmit, including fungi, viruses, rickettsiae, bacteria, and protozoa (Sauer et al. 1995). Additionally, these parasites can cause severe toxic conditions, irritation, and allergy in their hosts. Approximately 10% of the world Ixodid fauna is associated with domestic animals, especially livestock (Hoogstraal 1985). These

0022-2585/03/0268Ð0274$04.00/0 䉷 2003 Entomological Society of America

May 2003 Table 1.

SZABO´ ET AL.: TICKS ON WILD MARSH-DEER FROM BRAZIL

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Marsh deer populations evaluated for tick sampling in the marshes by the Parana´ river, Brazil

Deer group

No. of animalsa

Date of capture

Coordinateb/statea

Temporal relation to lake formation

Marsh highest width (km)

Approximate distance of captured animals from farms (km)

1 2 3 4

63 38 09 25

JuneÐJuly, October 1998 JuneÐJuly 1998 September 1998 February 2001

21⬚50⬘S, 52⬚13⬘W/MS 22⬚03⬘S, 52⬚21⬘W/MS 21⬚45⬘S, 51⬚58⬘W/SP 21⬚45⬘S, 52⬚14⬘W/MS

Prior Prior Prior After

13 10 7 5.5

7.5Ð13 2.5Ð10 0Ð2.5 0Ð5.5

a

Means only those animals systematically examined for ticks. Coordinate of one representative animal for the group. MS, Mato Grosso do Sul; SP, Saõ Paulo. b

ticks have been, obviously, studied in more detail. However, much less is known about ticks on wild animals, especially in their natural environment. Many times the original parasiteÐ host interactions are not known because they might have been overshadowed by newly established relationships (Tatchell 1987). Indigenous or naturally occurring parasitic or infectious life forms have had a common evolutionary history with their hosts in a speciÞc habitat, and this has led to a reduction or a cessation in detrimental effects (Malan et al. 1997), thus allowing survival of the involved species. Mechanisms exist in well-established hostÐparasite relationships to limit parasite numbers to tolerable levels. Ticks are no exception to this rule, and populations are only likely to be overwhelmed by tick infestation as a result of human activities (Tatchell 1987). Under human inßuence, an unbalanced environmentÐ hostÐparasite relationship is likely to occur. In practical terms, it means that sudden environmental changes for wild animals may occasionally be associated with sudden burdens of ectoparasites and/or higher pathogenicity induced by these parasites. A recently described violent outbreak of cat ßea (Ctenocephalides felis felis) infestations at a marsh deer quarantine exemplify such a situation (Szabo´ et al. 2000). However, wild animal parasites may occasionally spread to domestic animals and determine signiÞcant losses in animal husbandry. The marsh deer is the biggest cervid species of South America. Males can weigh as much as 150 kg (Duarte and Merino 1997). It is endangered throughout its range. The species is adapted to wetlands and other environments prone to ßooding, which unfortunately, are among the most degraded by the lakes of hydroelectric power stations. The population of this deer species, originally widespread in South America, has suffered a considerable decline and fragmentation (Tomas et al. 1997). Efforts to preserve this mammal are ongoing, and information about its life in the wild will be needed. Basic physiologic data such as reproductive cycle of males and females and social behavior or knowledge about infectious and parasitic diseases are still lacking. The present work describes the evaluation of tick infestations of free-living marsh deer populations before and after lake formation from a hydroelectric power station.

Materials and Methods Location and Animal Capture. Porto-Primavera hydroelectric power station is located in Brazil between the southwest of the state of Saõ Paulo and the east of the state of Mato Grosso do Sul (22⬚25⬘77⬙S; 52⬚58⬘84⬙W). Its water reservoir, Þlled up by the Parana´ river, ßoods an area of 2,200 km2 at the border of the two states. Before and after ßooding, marsh deer, Blastocerus dichotomus (Illiger), were captured for a wide range research program under the Þnancial support of Saõ Paulo State Energy Company (CESP). Wresting (bulldogging) technique, with the aid of a helicopter, was used for the capture of deer, as described by Duarte et al. (2001). Deer capture location was individually determined with the aid of a global positioning system (GPS) apparatus. A total of 247 animals were captured. Because these animals were subjected to different research and conservational projects for distinct purposes, only 135 animals could be systematically examined for tick infestations, which comprised the deer sample of the current study. Tick Sampling. All 135 animals were anesthetized with varying protocols (details to be published elsewhere) when they were examined for the presence of ticks. Because other biological samples (blood, feces, semen, fur, and skin) were simultaneously obtained for other studies, we conveniently adopted a 3-min period of tick evaluation on the whole left side of the body of each animal, when representative samples of 30 Ð 40 ticks were randomly collected all over the deer half-body and stored in 70⬚C ethanol until identiÞcation in laboratory. When ⬍30 ticks where found on a deer, all visible ticks were collected. Because of the Þeld time restriction on each animal, intensity of tick infestation on deer was visually scored at semiquantitative levels as follows: 0, no ticks found; ⫹, 1Ð10 ticks; ⫹⫹, 11Ð100 ticks; and ⫹⫹⫹, ⬎100 ticks, with no distinction of tick species or stage. Deer Groups. The original marsh deer population by the Parana´ river was estimated to be ⬇1,000 animals (Pinder 1996). Anesthetized animals, thoroughly examined for ticks, were captured on marshes alongside a 100-km course of the river and were allocated into four groups (groups 1, 2, 3, and 4) according to capture location and temporal relation to the lake formation (before and after). Groups and related information are presented on Table 1 and illustrated by satellite images on Fig. 1.

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Fig. 1. Satellite images showing the localities of marsh deer captured in the marshes by the Parana´ river, Brazil. Each white spot represent an individual captured for the study. (A) Capture sites at 1998, before lake formation. (B) Same area after initial ßooding, in 2001. G1, group 1; G2, group 2; G3, group 3; G4, group 4, MS, Mato Grosso do Sul State; SP, Saõ Paulo State.

Animals from groups 1 and 2 were captured at Mato Grosso do Sul State during 1998, before the drowning of the marsh for the hydroelectric power station. These groups were 13 km apart. Group 1 was in a marsh slightly wider than that of group 2. Animals from these two groups are supposed to have had little contact with farms before ßooding because of their living range. Under normal conditions, deer males have a living range of ⬇4,500 m2 and females of 2,000 m2 (Pinder 1995). Animal samples from the same place of these two groups received radio collars, and their movements were followed (Piovezan et al. 2001a). No movement between these two groups was observed before ßooding, and sampled deer remained close to their capture site. After the lake formation, however, deer range increased approximately three-fold on average; this was very variable among individuals (Piovezan et al. 2001a). Most of group 1 and 2 habitats were drowned, and initial observations showed that global deer population by the dam decreased, despite increased deer density in the remnants of the marsh (Andriolo et al. 2001). Animals from group 3 were also captured during 1998, before marsh drowning, when they were already living in a thin marsh and very close to farms. These animals were captured on the Saõ Paulo State side of the river and were 25 km away from group 1. Animals from this group were in an area that suffered minor area shrinkage caused by the dam, and thus, individuals tended to remain at their original site even after the formation of the lake (Piovezan et al. 2001b). Group 4 refers to animals captured in Mato Grosso do Sul State during 2001, 2 yr after ßooding. This group

included individuals from the area where animals from groups 1 and 2 lived. These animals lost their habitat because of inundation, and they moved to the remnants of the marsh, where they agglomerated close to farms (Piovezan et al. 2001a). Tick infestation levels on the four deer groups, with no distinction to tick species, were compared by the Kruskal-Wallis test, and means were compared by DunnÕs Multiple comparison test. During tick collection, two Boophilus microplusÐ engorged females collected from two marsh deer were taken alive to the laboratory and held at constant temperature of 29⬚C, 80 ⫾ 5% RH, and a 12:12 (L:D) photoperiod, for oviposition. Hatching rates of eggs were visually estimated in a stereoscope microscope, according to Labruna at al. (2000). Voucher tick specimens collected on this study have been deposited in the CNC-FMVZ/USP National Tick Collection, University of Saõ Paulo, SP, Brazil (accession numbers: 434, 435, and 451). Results Tick Species. Four tick species were found on the free-living marsh deer immediately after capture: Amblyomma cajennense (F.), Amblyomma triste (Koch), Anocentor nitens (Neumann), and B. microplus (Canestrini). Percentage of animals infested with each tick species is shown in Fig. 2. B. microplus was the most prevalent species on the four marsh deer groups. Groups 1, 2, 3, and 4 had 30.2, 44.7, 100.0, and 96.0% of animals carrying this tick species, respectively. The second most prevalent tick,

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Fig. 2. Percentage of marsh deer (n ⫽ 135) infested with each tick species after capture near the Porto-Primavera hydroelectric power station lake in Brazil.

A. triste, was observed on 15.9, 21.1, 22.2, and 88.0% of deer from groups 1, 2, 3, and 4, respectively. A. nitens and A. cajennense were observed on 32.0 and 16.0%, respectively, of only group 4 animals and always in very low numbers. Mixed infestations included mostly B. microplus and A. triste. All A. cajennense– and A. nitens–infested deer were also infested by B. microplus and A. triste. Preferential attachment sites of each tick species could not be determined because of the reduced time allowed for tick sampling. However, it is noteworthy that A. nites adult ticks were found attached in the preorbital lacrimal pit on three of eight deer infested by this tick species. Tick Infestation Levels. Tick infestation levels, evaluated by scoring, are presented in Fig. 3. Groups 1 and 2 had only 4.8 and 6.1%, respectively, of animals with

⬎100 detected ticks (⫹⫹⫹). No ticks (0) were found on almost one-half of these groups (group 1: 46.8%; group 2: 45.5%). However, groups 3 and 4 had much higher infestation levels, with 77.8 and 50.0% of the animals, respectively, presenting score ⫹⫹⫹ and lacking noninfested animals (0). Infestation levels of groups 3 and 4 were signiÞcantly higher than those of groups 1 and 2 (P ⬍ 0.001). In general, captured animals were healthy, and no correlation could be observed between high tick infestation levels and disease. One of the B. microplusÐ engorged female weighed 333 mg and furnished an egg mass of 180 mg, from which 50% of the eggs hatched. The other female tick also oviposited, but its eggs began to hatch before we weighed them. Nevertheless, a 99% hatching was obtained.

Fig. 3. Tick infestation levels of marsh deer (n ⫽ 135) captured near the Porto-Primavera hydroelectric power station lake in Brazil. Infestations were evaluated by scores: 0, no ticks found; ⫹, 1Ð10 ticks; ⫹⫹, 11Ð100 ticks; and ⫹⫹⫹, ⬎100 ticks.

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JOURNAL OF MEDICAL ENTOMOLOGY Discussion

Investigation of ticks on marsh deer before and after the formation of the lake from the hydroelectric power station displayed some important observations. The main tick species recovered from this host was B. microplus, the most common cattle tick in Brazil. This tick species was introduced in Brazil with cattle (Aragaõ 1911) and is believed to have been originally parasite from forest dwelling Artiodactyla in Southeast Asia (Tatchell 1987). Cattle are currently recognized as the only primary host for B. microplus in Brazil (Labruna et al. 2001), and thus these bovines at the studied area must have been the infestation source of B. microplus for the marsh deer. It is worthwhile to mention that marsh at this area is mostly neighbored by dairy and beef cattle farms. Moreover, marsh deer have been repeatedly seen on cattle pastures in the studied area, and cattle were seen pasturing at the periphery of the marsh (J.M.B.D., unpublished data). Such a territorial overlap can unquestionably be blamed for B. microplus infestations of deer. What is still a doubt is whether the marsh deer is able to act as primary host for B. microplus, and therefore, maintain a tick population by itself, or if cattle are needed as a constant source to maintain this tick species population. In the current study, we collected two fertile B. microplusÐ engorged females from two marsh deer. These results might indicate marsh deer as a permissive host for B. microplus establishment, but more data would be needed for conclusive observations. In this regard, previous studies with other deer species have shown that deer-exposed Boophilus ticks displayed lower biological and reproductive performance than cattle-exposed ticks (De la Vega 1984, Cooksey et al. 1989, Davey 1990, Barre et al. 2001). Although these results suggest that deer cannot act as primary hosts for B. microplus, there is a lot of controversy about the potential of white-tailed deer (Odocoileus virginianus L.) to sustain B. microplus populations without the coexistence of cattle (Davey 1990). However, it is possible that the marsh environment acts as a natural barrier for the development of the nonparasitic stages of B. microplus, and this tick species would disappear in the absence of cattle. Whatever the case, it is a fact that marsh deer can suffer B. microplus infestations when living close to cattle and are potentially exposed to blood losses and infectious agent vectoring by this tick. Thus, considering the initial observations on B. microplus infestations of marsh deer, as described in this paper, this tick species might represent a potential threat and warrants further studies for correct management of marsh deer in the future. The second most common tick on marsh deer, A. triste, was initially misidentiÞed as Amblyomma tigrinum Koch (Szabo´ et al. 2000). Careful assessment of A. triste identiÞcation is needed because it closely resembles Amblyomma maculatum Koch and A. tigrinum. The main distinctive character of A. triste is the presence of a small tubercle at the postero-internal angle of all festoons except at the middle one in both sexes (Kohls 1956). As far as we know, there have been

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only a few host records of A. triste in Brazil. The Þrst one was from a tapir (Tapirus sp.) (Kohls 1956), and later from a dog (Freire 1967), an opossum (Didelphis marsupialis) (Lemos et al. 1997), and a capybara (Hydrochaeris hydrochaeris) (Sinkoc et al. 1997). Conversely, this tick has been extensively reported on dogs and humans in Uruguay, where it is believed to vector a cutaneous-ganglionar rickettsiosis to humans (Conti-Dõáz 2001, Venzal et al. 2001). Although ticks in the current study were collected in different periods of the year, during summer, spring, and winter months, no immature Amblyomma ticks were found on deer compared with A. triste adult ticks, which were found in all surveyed months. Another study conducted simultaneously to the present one evaluated ticks infesting wild animals captured at the Porto-Primavera hydroelectric power station area (same location of the current study) (Labruna et al. 2002b). These animals included 48 wild mammals other than deer, comprised of 11 different species, including anteaters, carnivores, peccaries, capybaras, and primates. In this study, only one adult specimen of A. triste was found on wild mammals other than marsh deer. Moreover, hundreds of Amblyomma spp. immature ticks from these wild hosts were reared until the adult stage in laboratory, but none molted to A. triste. These data show evidence of marsh deer as the most important host for the A. triste adult stage in the studied area, but do not explain the obscurity of hosts for A. triste immature stages in the same area. In Uruguay, marsh deer are now extinct (Tomas et al. 1997), but adults of A. triste are commonly found on dogs and humans (Conti Dõáz 2001, Venzal et al. 2001). Small mammals such as marsupial (Monodelphis dimidiata) and rodents (Scapteromys tumidus, Oxymycterus nasutus, and Oligorysomys flavescens) have been found naturally infested by immature stages of A. triste in Uruguay (Venzal and Fregueiro 1999). These data suggested that A. triste immature stages prefer small mammals for feeding, whereas the adult stage has predilection to larger mammals. Further studies should evaluate the role of small mammals as hosts for A. triste immature stages and dogs for the adult stage in the present studied area of Brazil, where marsh deer seems to be the primary hosts for the adult stage. A. nitens and A. cajennense were the less abundant ticks and were only found on marsh deer captured after the lake formation. A. nitens is primarily a horse parasite in Brazil, whereas A. cajennense uses horses and other wild hosts (tapirs, capybaras) as primary hosts for all parasitic stages (Labruna et al. 2002a). These other hosts, especially horses, could be the sources of infestation for marsh deer. It is possible that the lake formation have pushed deer toward farm pastures or other nonmarsh areas and increasingly exposed this host to these tick species. Ticks previously reported from marsh deer include B. microplus (Freire 1972, Serra-Freire et al. 1996, Pereira et al. 2000), A. tigrinum (Serra-Freire et al. 1996, Pereira et al. 2000), and A. cajennense (Pereira et al. 2000). Careful reexamination of the tick specimens

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collected on marsh deer in the study of Pereira et al. (2000) indicated that the A. tigrinum samples were in fact A. triste (M.B.L. and M.J.P.S., unpublished data). These specimens were deposited in the Tick Collection CNC-FMVZ/USP (accession number: 699). The adult stage of A. tigrinum is primarily a parasite of carnivores, especially dogs, but rarely infests herbivores (Guglielmone et al. 1982). Its presence on marsh deer, as described in the above studies, may indicate a behavior alteration or an unknown feature of the tick. However, because of its morphological similarity to A. triste, revision of the identity of the samples collected from Cervidae may be worthwhile. Infestation levels of deer groups 3 and 4 were signiÞcantly higher than those of groups 1 and 2. Several factors could be responsible for such differences. Seasonal activity of ticks, especially of the most ubiquitous, B. microplus, is one of them. Unfortunately tick sampling of deer groups was subordinated to deer capture scheme determined by several other projects and logistic background (e.g., helicopter availability) and thus could not be done sequentially in the same seasons. It should be mentioned, however, that B. microplus may develop as many as four generations per year in the Southeast region of Brazil (Cordove´ s 1997), which allows for high infestation rates all year. It should also be noted that tick sampling from animals from groups 1 and 3 somewhat overlapped temporarily, suggesting a decreased inßuence of seasonal activity of ticks on the observed differences. However, a comprehensive study is still not at the disposal of all municipalities of this region, and the inßuence of seasonal factors on tick infestation intensity cannot be discarded. In our present view, however, the main possible factor to determine higher infestation levels of marsh deer could be the shrinkage of the marsh, and therefore, a higher rate of sharing of pastures infested by cattle with B. microplus. In the case of group 3, evaluated before lake formation, the highest infestation scores (Fig. 3) could be linked to the fact that deer were scattered in a narrow marsh in close proximity to farms (Fig. 1; Table 1). Members of group 4, also displaying high infestation levels, were examined after lake formation. These animals were pushed toward farms by the lake and were captured in the summer at the narrow remnants of the marsh (Table 1). Thus, the close proximity to and forced coexistence with cattle from groups 3 and 4 marsh deer might explain the high infestation levels by B. microplus. It is also important to observe that the rate of A. tristeÐinfested marsh deer increased in animals captured after the lake formation. Groups 1Ð3 had ⬇15Ð20% of animals infested by this tick species, whereas group 4 displayed ⬎80% of animals with these ticks. Group 4 marsh deer, exposed to sudden habitat shrinkage, was composed of many displaced animals living in higher density (Andriolo et al. 2001). The higher density of deer and other wild animals from the marsh might have beneÞted ticks seeking wildlife, thus increasing A. triste infestation intensity of its host. The lake from a hydroelectric power station reduces the natural habitat of species, especially those

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living in marsh area, affecting wildlife in a multitude of ways. Animal populations can become more vulnerable and may decrease because of starvation, increased predation, stress-associated infections, and other factors, such as hunting. HostÐparasite relationships will also be altered, but its importance for wild animal survival is unknown. The present work indicates that habitat loss may substantially interfere with marsh deer tick infestations. Considering the potential of ticks for disease vectoring and directly harming hosts, the increase of infestation intensity and exposure to new tick species are a matter of concern if a more secure managing and conservation of marsh deer are to be achieved. Acknowledgments We thank Companhia Energe´ tica de Saõ Paulo (CESP) for Þnancial support and logistic collaboration, FAPESP for Þnancial support (M.P.J.S.), and IBAMA for kindly providing permission for the capture of animals. We thank J. M. Venzal (Uruguay) and A. A. Guglielmone (Argentina) for conÞrming the taxonomic identiÞcation of A. triste. We are also indebted to all technicians and volunteers who helped to capture and maintain animals.

References Cited Andriolo, A., U. Piovezan, M.J.R. Paranhos da Costa, J. Laake, and J.M.B. Duarte. 2001. Estimativa ae´ rea de abundaˆncia e distribuiç aõ do Cervo-do-Pantanal (Blastocerus dichotomus) na bacia do rio Parana´, entre as barragens de Porto Primavera e Jupia´ em avaliaç o˜ es pre´ e po´ s enchimento da primeira cota da UHE Se´ rgio Mota. In J.M.B. Duarte (ed.), O Cervo-do-Pantanal (Blastocerus dichotomus) de Porto Primavera. Funep, Jaboticabal SP, Brazil. Araga˜ o, H. 1911. Notas sobre ixo´ didas brazileiros. Mem. Inst. Oswaldo Cruz. 3: 145Ð195. Barre, N., M. Bianchi, and L. Chardonnet. 2001. Role of Rusa deer Cervus timorensis russa in the cycle of the cattle tick Boophilus microplus in New Caledonia. Exp. Appl. Acarol. 25: 79 Ð96. Cooksey, L. M., R. B. Davey, E. H. Ahrens, and J. E George. 1989. Suitability of white-tailed deer as hosts for cattle fever ticks (Acari: Ixodidae). J. Med. Entomol. 26: 155Ð 158. Conti-Dıáz, I. A. 2001. Rickettsiosis por Rickttsia conorii (Þebre botonosa del Mediterrańeo o Þebre de Marsella). Estado actual en Uruguay. Rev. Med. Uruguay. 17: 119 Ð 124. Cordove´s, C. O. 1997. Carrapato: controle ou erradicaç aõ. Livraria e Editora Agropecua´ria Ltda, Guaõ´ba RS, Brazil. Davey, R. B. 1990. Failure of white-tailed deer, Odocoileus virginianus L. to sustain a population of cattle ticks, Boophilus annulatus (Say), through sucessive generations. J. Parasitol. 76: 356 Ð359. De la Vega, R. 1984. Aspectos del desarollo de la garrapata del ganado vacuno (Boophilus microplus) sobre el venado de cola blanca (Odocoileus virginianus). Rev. del Salud Animal. 6: 59 Ð 64. Duarte, J.M.B., and M. L. Merino. 1997. Taxonomia e evoluç aõ, pp. 2Ð21. In J.M.B. Duarte (ed.), Biologia e conservaç aõ de cervõ´deos Sul-Americanos: Blastocerus, Ozotoceros e Mazama. Funep, Jaboticabal SP, Brazil. Duarte, J.M.B., M. L. Merino, S. Gonzales, A.L.V. Nunes, J. M. Garcia, M.J.P. Szabo´ , J. R. Pandolfi, I. G. Arantes, A. A.

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