Exp Appl Acarol (2010) 50:169–179 DOI 10.1007/s10493-009-9294-7
Ticks (Acari: Ixodidae) within various phytophysiognomies of a Cerrado reserve in Uberlaˆndia, Minas Gerais, Brazil Viviane Aparecida Veronez Æ Beatriz Zanolli Freitas Æ Maria Marlene Martins Olega´rio Æ William Mendes Carvalho Æ Graziela Virginia Tolesano Pascoli Æ Khelma Thorga Æ Marcos Vale´rio Garcia Æ Matias Pablo Juan Szabo´ Received: 1 April 2009 / Accepted: 14 July 2009 / Published online: 20 August 2009 Ó Springer Science+Business Media B.V. 2009
Abstract Cerrado biome, the South American savannah, covers about 2 million km2 and is very rich in endemic species but threatened by agriculture. In this report free-living tick species are presented, and their seasonal and relative distribution within the various phytophysiognomies in a small Cerrado reserve in Minas Gerais State, Brazil. Overall 2,694 free-living ticks were found during a 2 years sampling period with CO2 traps and cloth dragging. Of these, 73.5% were Amblyomma cajennense and 0.6% Amblyomma dubitatum. All other ticks (25.9%) were retained as Amblyomma spp. Adults of A. cajennense peaked in spring, the nymphs in winter of both years. Amblyomma larval clusters were found in autumn and winter. Adult ticks (46.7%) and nymphs (39.5%) were most often found in woodlands, whereas most larval clusters were found in valley-side marshes (39%). Amblyomma cajennense, Anocentor nitens, Rhipicephalus (Boophilus) microplus and Rhipicephalus sanguineus ticks were found on domestic animals from neighboring properties. Search for Rickettsia in the hemolymph of 497 A. cajennense and one A. dubitatum ticks yielded negative results. Results confirmed earlier reports on the overwhelming prevalence of A. cajennense ticks in the Cerrado biome of Brazil and added information to habitat preferences of this tick species, a major vector in Brazil of the Rocky Mountain spotted fever. Keywords Ixodidae Cerrado Amblyomma cajennense Seasonality Brazil Phytophysiognomy
V. A. Veronez M. V. Garcia Faculdade de Cieˆncias Agra´rias e Veterina´rias, Universidade Estadual Paulista, Jaboticabal, SP, Brazil B. Z. Freitas M. M. M. Olega´rio W. M. Carvalho G. V. T. Pascoli K. Thorga M. P. J. Szabo´ (&) Laborato´rio de Ixodologia, Faculdade de Medicina Veterina´ria da Universidade Federal de Uberlaˆndia, Av. Para´, 1720, Campus Umuarama-Bloco 2T, Uberlaˆndia, MG CEP 38400-902, Brazil e-mail:
[email protected]
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Introduction The Cerrado Biome of tropical South America covers about 2 million km2, representing ca. 22% of the land surface of Brazil, plus small areas in eastern Bolivia and northwestern Paraguay (Oliveira-Filho and Ratter 2002). The whole biome is characterized by an extremely variable physiognomy, ranging from open grassland to forest with a discontinuous grass layer. Between these two extremes lies a continuum of savanna formations spanning the entire range of woody plant density, referred to collectively as the cerrados (Oliveira-Filho and Marquis 2002). The Portuguese word cerrado means ‘‘halfclosed,‘‘ ‘‘closed,’’ or ‘‘dense,‘‘ and the name is particularly appropriate because this vegetation is neither open nor closed (Eiten 1972). Cerrado is considered a biodiversity hot spot which means that it is especially rich in endemic species and particularly threatened by human activities (Cincotta et al. 2000). Information of ticks from this biome is still scarce and apart from a few reports (Knight 1992; Campos Pereira et al. 2000; Bechara et al. 2002; Szabo´ et al. 2007a) no systematic study was undertaken. The Cerrado is increasingly exposed to agricultural activities which have a direct impact on host–parasite relationships. The consequences of the mixing of parasites from rural, urban and wildlife areas are still unknown while at the same time, reemerging and recently recognized tick-borne pathogens are a matter of concern in Brazil (Galva˜o et al. 2005; Silveira et al. 2007; Machado et al. 2006). In this report ticks within various phytophysiognomies of a small Cerrado reserve surrounded by agricultural activities in Uberlaˆndia, Minas Gerais, Brazil is presented. Ticks from domestic animals from lands neighboring the reserve are also reported to evaluate the tick exchange between rural and wildlife areas.
Materials and methods Study site This study was conducted from June 2006 to December 2008 at a small (404 ha) Cerrado reserve named ‘‘Estac¸a˜o Ecolo´gica do Panga’’ and surrounded by land used for agricultural activities. The reserve is located in Uberlaˆndia municipality, Minas Gerais State, Brazil (19°100 S, 48°230 W, 800 m of altitude), 30 km south from the city centre. The region is characterized by a subtropical climate with two well defined seasons: a dry winter (May to September) and a rainy summer (October to April). The mean annual temperature and precipitation are 22°C and 1,650 mm, respectively. It roughly corresponds to ecological unit 3A according to a recent classification of the environmental and ecological diversity of the Cerrado region of Brazil (Silva et al. 2006). In this unit, plains with some rolling terrain, dominate the landscape. Native vegetation is a mosaic of semi-deciduous forest and dense woodlands with some dense savanna. The ‘‘Panga’’ reserve itself is mostly covered by typical Cerrado physiognomies—from which cerrado sensu stricto is the dominant one, but forest physiognomies are also found, especially along the stream valleys. Many species of vertebrate animals are known to exist in the reserve. Apart from several birds, reptiles, amphibians and small rodents, and according to a recent survey (Guimaraes et al. 2008) and our own field observations the following animals were detected in the reserve: White-eared Opossum (Didelphis albiventris), Black-pencilled Marmoset (Callithrix penicillata), Black-striped Capuchin (Cebus libidinosus), Maned Wolf (Chrysocyon brachyurus), Crab-eating Fox (Cerdocyon thous), Coati (Nasua nasua), Crab-eating
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Raccoon (Procyon cancrivorus), Tayra (Eira barbara), Gray Brocket Deer (Mazama gouazoubira), Pampas Deer (Ozotoceros bezoarticus), Collared Peccary (Pecari tajacu), Lowland Paca (Cuniculus paca), Tapeti (Sylvilagus brasiliensis), Nine-banded Armadillo (Dasypus novencinctus), Six-banded Armadillo (Euphractus sexcinctus), Southern Nakedtailed Armadillo (Cabassous unicinctus), Giant anteater (Myrmecophaga tridactyla), Collared Anteater (Tamandua tetradactyla), Jaguarundi (Puma yaguarondi), Cougar (Puma concolor), Ocelot (Leopardus pardalis), and Capybara (Hydrochoerus hydrochaeris). Of these species collared peccary seemed to be the most abundant one, whereas capybaras were detected only by feces in the gallery forest, as well as pampas deer which was also determined by traces. Domestic animals were not allowed in the reserve, however, cattle occasionally and dogs frequently invaded it. Tick sampling Ticks were collected eight times and every season from June 2006 to January 2008 in 13 different locations within the reserve. Locations were chosen to include various phytophysiognomies of the Cerrado (Table 1). Sampling included capture of free-living ticks and collection of ticks from domestic animals from neighboring properties. Free-living ticks were captured using CO2 traps and cloth dragging. CO2 traps were used as previously described (Oliveira et al. 2000). Larvae found on each CO2 trap were considered to belong to a single cluster. Dragging was performed as described by Rechav (1982) but slightly modified. Briefly, the drag was Table 1 Locations, coordinates and altitude, phytophysiognomies and number of CO2 traps used for tick sampling in the Cerrado biome of Uberlaˆndia, Minas Gerais State, Brazil, 2006–2008 Location
Coordinates
1
19°100 55.500 S; 48°240 08.400 W
Altitude (m)
Cerrado phytophysiognomies (Oliveira-Filho and Ratter 2002)
Number of CO2 traps used
823
Cerrada˜oa
20
2
19°10 0.69 S; 48°23 29.6 W
760
Gallery forestb
10
3
19°100 08.500 S; 48°230 2600 W
756
Campo sujoc
10
4
19°100 56.200 S; 48°230 38.800 W
795
Veredad
16
5
19°100 56.200 S; 48°230 38.800 W
795
Cerrada˜o
10
6
19°100 50.400 S: 48°230 40.100 W
778
10
7
19°100 46.600 S; 48°230 48.300 W
816
Gallery forest Cerrada˜o
8
19°100 24.900 S; 48°230 47.800 W
802
Cerrado sensu strictoe
10
9
19°100 13.500 S; 48°230 34.0800 W
790
Cerrada˜o
10
10
19°110 13.700 S: 48°240 16.100 W
804
Vereda
10
11
19°100 43.600 S: 48°220 41.700 W
780
Gallery forest
10
12
19°100 49.300 S: 48°230 32.300 W
790
Campo sujo
10
13
19°100 43.600 S: 48°220 41.700 W
759
Gallery forest
0
00
0
00
10
5
a
Almost closed woodland with crown cover of 50–90%, made up of trees, often of 8–12 m or even taller, casting a considerable shade so that the ground vegetation layer is much reduced
b
Narrow forest strips found along streams and flanked by grasslands or Cerrados
c
Grassland with a scattering of shrubs and small trees
d
Valley-side marshes where the water table reaches or almost reaches the surface during the rainy season
e
Vegetation dominated by trees and shrubs often 3–8 m tall and giving more than 30% crown cover but with still a fair amount of herbaceous vegetation between them
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pulled for 20 min by each of two persons simultaneously in a random fashion at each sampling site. During this period the cloth was examined for ticks approximately every 20 m of dragging. Dragging was not possible in spots 1, 6, 7, 9, 10 and 11 either because of the dense vegetation or due to the high humidity/flooding of the sampled area. Sampling of free-living ticks at each season occurred repeatedly at the same location and with a similar number of CO2 traps and dragging time. Details on tick sampling locations are presented in Table 1. All ticks were brought to the laboratory, where they were counted. Adults and nymphs were counted individually. For convenience, we considered each larval cluster as a larval unit for counting. At each sampling expedition, a variable number of domestic animals from neighboring properties were examined for tick infestations. Since only two tick species were found host questing during the above mentioned period, additional random tick collections were performed in May, August and December 2008. A mean number of, approximately, 35 CO2 traps as well as cloth dragging were used at each collecting period in new locations within Valley-side marshes, Cerrada˜o and Gallery forest phytophysiognomies. Nocturnal sampling Since the Cerrado may be very dry and hot during the diurnal period, a possible increase in the tick host questing activity at night was investigated in location 8 (Cerrado sensu stricto). For this purpose cloth dragging as described above, was performed in a 400 m course in the daylight and the very same course sampled after sunset. Such procedure was done for a year, once in each season and temperature and relative humidity were measured during some of the samplings. Tick sampling on trees and nests The possible infestation site of birds was investigated by placing modified CO2 traps on trees. CO2 traps for this purpose were made of small 250 ml disposable plastic cups containing, approximately, 100 g of dry ice nuggets. External surface of the cup was surrounded by an adhesive type to trap ticks attracted to the cup. Such traps were placed on trees, mostly buriti-palms (Mauritia flexuosa), 6–10 m above the ground and inspected after 1.5–2 h. This procedure was performed with seven traps in the spring of 2006, eight traps in the summer of 2007 and five traps in the autumn of 2007. In the summer of 2008 three traps were placed close to Great Kiskadee (Pitangus sulphuratus) nests on small trees, approximately 2 m above the ground, and one trap close to a Tanager (Thraupis sp.) nest on the roof of the caretaker’s residence within the reserve. Tick identification Currently, it is impossible to perform a proper morphological taxonomic identification of the immature stages of the Amblyomma species from Brazil. Thus, the collected larvae and nymphs were brought alive to the laboratory at the Federal University of Uberlaˆndia, where attempts to rear them until the adult stage were performed by feeding them on tick-bite naı¨ve rabbits, as previously described (Labruna et al. 2002a). Adults obtained from the engorged nymphs were used for species identification of the former immature ticks. Adult ticks were identified into species using the taxonomic keys proposed by Barros-Battesti
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et al. (2006). The voucher tick specimens collected in the present study have been deposited in the CC-FAMEV/UFU Tick Collection, Federal University of Uberlaˆndia (accession numbers: 244, 444–447). Hemolymph test Search for Rickettsia species in ticks was performed with 497 A. cajennense and one Amblyomma dubitatum adult. For this purpose, each tick specimen was individually tested by the hemolymph test according to Burgdorfer (1970). Briefly, a drop of hemolymph collected from the broken leg of each tick, was spread onto a slide and then subjected to Gimenez staining (Gimenez 1964). The slide was then scrutinized under light microscopy for Rickettsia-like organisms, especially inside hemolymph cells.
Results Ticks were captured overwhelmingly by CO2 traps and 2,694 free-living ticks were found in the initial sampling period (Table 2). Of these, 1,981 (73.5%) were A. cajennense and 16 (0.6%) A. dubitatum. All other ticks were retained as Amblyomma spp. (n = 697/25.9%) and were either larvae or nymphs that died before reaching the adult stage in the laboratory, precluding proper species identification. Additional random sampling yielded 118 ticks, 95 adults and 16 nymphs of A. cajennense and seven Amblyomma sp. nymphs. Random collection of these ticks precluded their use for seasonal or relative distribution at each phytophysiognomy. Seasonal distribution could be determined for A. cajennense ticks, the only species found in high numbers. Adults of A. cajennense peaked in spring, nymphs in winter of both years (Fig. 1). None of the larval clusters could be bred until the adult stage. Of these, ten clusters were found in autumn 2006, five in autumn 2007 and two in winter 2007. Relative distribution of ticks at each phytophysiognomy within the Cerrado biome was calculated based on the mean number of ticks attracted to each CO2 trap (Fig. 2). Most of the adult ticks (46.7%) were found in the woodland (Cerrada˜o) fewer adults were found in traps from grassland (Campo sujo—9.3%) and Cerrado sensu stricto (5.4%). In the case of nymphs most ticks were in the woodland (39.5%) and only 9.7% in valley-side marshes. Most larval clusters were found in the valley-side marshes (39%) whereas only 8.5% were found in the grassland. All A. dubitatum ticks were found in location 6, a gallery forest. Nocturnal tick sampling by drag yielded only five nymphs of A. cajennense, all in the winter of 2007 (Table 3). Diurnal dragging at the same location yielded no tick. Temperature decreased and relative humidity increased from day to night. During the day
Table 2 Number of ticks and species found in the Cerrado biome, Uberlaˆndia, Minas Gerais State, Brazil, 2006–2008
Tick species
Adults Amblyomma spp. Amblyomma cajennense
a
Larvae found on one trap were considered to belong to one larval cluster
Number of ticks
Amblyomma dubitatum Total
Nymphs
Larval clustersa
Total
–
680
17
697
1,157
824
0
1,981
1
15
0
16
1,158
1,519
17
2,694
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450 Nymphs
A. cajennense tick numbers
400
Adults
350 300 250 200 150 100 50
Summer 2008
Spring 2007
Winter 2007
Autumn 2007
Summer 2007
Spring 2006
Winter 2006
Autumn 2006
0
Fig. 1 Seasonal distribution of Amblyomma cajennense ticks in the Cerrado biome of Uberlaˆndia, Minas Gerais State, Brazil, 2006–2008
50 45 40
% of ticks
35 30 25 20 15 10 5 0 Cerradão
Gallery forest Larva
Campo Sujo Nymph
Vereda
Cerrado "sensu stricto"
Adult
Fig. 2 Relative distribution of Amblyomma ticks in the various phytophysiognomies of the Cerrado biome of Uberlaˆndia, Minas Gerais State, Brazil, 2006–2008
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Table 3 Tick sampling by cloth dragging during the day and in the same location at night in the Cerrado biome (Cerrado sensu stricto) Season
Spring 2006
Sampling time
Temperature and relative humidity in the shadow
Temperature and relative humidity outside the shadow
Ticks collected
–
10:30
–
–
21:30
–
–
–
Summer 2007
14:00
26°C and 66%
[51°C and \24%a
–
20:00
23°C and 99%
23°C and 99%
–
Autumn 2007
14:00
24°C and 64%
46°C and 24%
–
19:30
16.1°C and 72%
–
–
Winter 2007
a
08:00
23.9°C and \24%
28.4°C and \24%
–
19:30
15.8°C and 24%
15.8°C and 24%
A. cajennense (5 nymphs)
Temperature and humidity overcame thermohygrometer measuring limits
temperature and humidity differed drastically between spots under the vegetation shadow and those a few centimeters away but exposed to the sunlight. In summer 2007, for example, temperature and humidity at 14:00 was of, respectively, 26°C and 66% in the shadow, while [51°C and \24% in the sun, respectively. At night (20:00) differences between such spots were not detected. From 56 domestic animals 379 ticks were collected. Dogs (n = 25) harbored 26 adults and two nymphs of Rhipicephalus sanguineus and one adult and 18 nymphs of A. cajennense. From horses (n = 11) 45 adults of A. cajennense, 78 adults and six nymphs of Anocentor nitens, 13 adults and two nymphs of Rhipicephalus (Boophilus) microplus and three nymphs and one larvae of Amblyomma sp. were recovered. On cattle (n = 20) four adults of A. cajennense and 179 adults and one nymph of R. (B.) microplus were found. Tick sampling on trees and nests yielded negative results and no Rickettsia was seen in the hemolymph of ticks.
Discussion Of the two tick species found in the Cerrado reserve, A. cajennense was by far the most abundant and shows its adaptation to this biome. In fact, the prevalence of A. cajennense over other tick species elsewhere in Brazil, with the exception of the rainforests, has been reported before (Campos Pereira et al. 2000; Labruna et al. 2002a, 2005; Estrada-Pen˜a et al. 2004; Szabo´ et al. 2007a, b; Canc¸ado et al. 2008). Dominance of A. cajennense is a meaningful finding if one considers that this parasite is very aggressive to humans and is in Brazil the most common vector associated with spotted fever, caused by the bacterium Rickettsia rickettsii (Guedes et al. 2005; Sangioni et al. 2005; Guglielmone et al. 2006). In this regard lack of Rickettsia in the hemolymph of ticks from the reserve must be seen with some caution and cannot be regarded as a definitive result. Many false negative results may occur and even in spotted fever endemic areas R. rickettsii may be difficult to detect (Estrada et al. 2006) thus further investigation in the reserve is warranted. Tapirs, capybaras and horses are considered primary host species for the adult stage of A. cajennense in Brazil (Labruna et al. 2001). However, there were no tapirs and horses
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in the reserve and capybaras were in numbers too low to maintain high environmental infestation. At the same time a big group of peccaries was frequently seen in the reserve and signs of these animals (revolved soil) in the cerrada˜o and marshes were associated with high tick infestation levels. In this regard Labruna et al. (2005) suggested peccaries may be another primary host for adult A. cajennense ticks. Anteaters, seen in the reserve as well, are also known to harbor A cajennense adults sometimes in high infestation levels (Campos Pereira et al. 2000; Bechara et al. 2002; Martins et al. 2004). These animals, however, are solitary and would hardly by themselves disseminate A. cajennense ticks over such a broad area. Thus peccaries are more likely to be the main host for A. cajennense tick populations within the reserve. Tick counts on several peccaries would be the way to assess such issue. The second species found, A. dubitatum (=Amblyomma cooperi), is a capybara tick (Labruna et al. 2004a). All A. dubitatum were found in its host preferred habitat within the Cerrado, the gallery forest. Capybaras have semi-aquatic habits (Reis et al. 2006) and gallery forests provide a water source, hiding and resting place. Rickettsia species has already been found in this tick species (Lemos et al. 1996; Labruna et al. 2004b). In fact A. dubitatum is capable to attach to man (Labruna et al. 2007a, b) but the overall significance of this behavior needs further evaluation. Tick species collected from domestic animals were those usually found in Brazil. Rhipicephalus sanguineus is the most common dog tick and may infest animals in both urban and rural areas (Szabo´ et al. 2001; Labruna et al. 2005). Rhipicephalus (B.) microplus is the cattle tick in the Neotropical region (Guglielmone et al. 2004) although other domestic and wild animals can be parasitized if sharing highly infested pastures (Labruna et al. 2002a, b; Szabo´ et al. 2003). A. nitens and A. cajennense are the most frequent species infesting horses on farms of the state of Sa˜o Paulo (Labruna et al. 2001, 2002b). A. cajennense ticks were found on dogs and cattle as well, indicating that these hosts had access to environment infested with this tick species. A. cajennense infestation source for domestic animals could be both infested pastures or nearby Cerrado fragments. In this regard those dogs that frequently invade the Cerrado reserve can be considered potential carriers of ticks from wildlife to both rural areas and humans. In a recent survey for ticks in the Cerrado (Szabo´ et al. 2007a) several hundred kilometers away, using a comparatively lower sampling effort and similar methodology other tick species such as Amblyomma parvum, Amblyomma nodosum and Amblyomma naponense were also found in the environment. Together these results suggest that the tick fauna in the Panga reserve is poor. On the other hand, sampling at inadequate/restricted spots is another possible reason for the low tick diversity found. Since birds from a small forest fragment close to Uberlaˆndia city were shown to harbor Amblyomma nodosum and Amblyomma longirostre ticks (Pascoli 2005), and Labruna et al. (2007b) suggested that A. longirostre would be an arboreal tick, CO2 traps were mounted on trees and bird nests. Unfortunately this sampling effort yielded negative results. Lack of ticks in nests and trees may be attributed to the relatively low capture effort, or inadequate methodology. Information on tick behavior in Brazil is still in its infancy and an array of tick host-questing sites as well as of stimulus that attracts ticks may occur. Perhaps CO2 traps might not be appropriate for several tick species of the Cerrado. Tick sampling in the reserve revealed an uneven distribution among the various phytophysiognomies of the Cerrado. Adults and nymphs were found in higher numbers in a forested formation (Cerrada˜o) whereas larval clusters predominated in marsh areas. Higher likelihood of finding hosts and moisture are probably responsible for such distribution of questing ticks within the reserve. Campo sujo (grassland) and Cerrado sensu stricto are
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drier phytophysiognomies with lower vegetation and a desiccating environment for host questing ticks during the day. On the other hand, low tick numbers in the gallery forests were an unexpected finding. Capybaras and a permissive environment close to water sources are usually responsible for very high A. dubitatum and A. cajennense tick infestations (Souza et al. 2006; Szabo´ et al. 2009). Low infestation at the reserve in such phytophysiognomy indicates decreased host availability for ticks. Indeed capybara signals such as feces and traces were rarely seen during the survey. The sampled gallery forests were close to the road, at the limits of the reserve and under strong anthropogenic effect; probably of illegal hunting. We speculate that such situation must have expulsed bigger mammals, including capybaras consequently decreasing tick infestations. Tick diversity as well as sampling within the various Cerrado phytophysiognomies might have also been influenced by tick circadian activities. Cloth dragging in particular is a sampling method that is effective for ticks seeking hosts on the vegetation. Since the Cerrado is very hot and, during the winter, very dry, it was supposed that host seeking activity of ticks in open phytophysiognomies is enhanced after sunset to avoid desiccation as well as to increase the likelihood of meeting those hosts that are more active at night. Sampling of ticks in the Cerrado sensu stricto after sunset yielded five A. cajennense nymphs only on one occasion whereas no tick was captured on the same site during the day. Even though this result might indicate that there is indeed an increase in tick activity after sunset further experiments with more trials and repeated sampling over all night should provide a better view of the real situation. Determination of seasonal activity was possible only for A. cajennense ticks. Peaks of nymphs in winter and of adults in spring indicate a similar seasonal activity to the 1-year generation pattern described for A. cajennense ticks in southeastern Brazil (Labruna et al. 2003; Szabo´ et al. 2007b). All larval clusters were found either in the autumn or winter which fits the aforementioned seasonal distribution of A. cajennense. Even though we could not identify larval clusters, overwhelming sampling of A. cajennense adults and nymphs in the reserve strongly suggests that most larvae were of the same species. On the whole such results indicate that seasonal activity of A. cajennense ticks in rural as well as natural environment is similar in southeastern Brazil. Results from this work showed a decreased diversity of tick species in the reserve which we attribute to a decrease in host diversity. The small size of the reserve and agricultural activities surrounding it do not leave room for hosts once abundant in the Cerrado biome such as Jaguars (Panthera onca) and Tapirs (Tapirus terrestris). At the same time conventional methods used for sampling free-living ticks have bias (Szabo´ et al. 2007a) and several other tick species may be present in the studied area at specific sites such as burrows and dens. Whatever the case A. cajennense tick abundance in the reserve habitat is unquestionable. This dominance can be attributed to both a wide range of adequate hosts as well as to forest fragments of the Cerrado which protect ticks against desiccation in the sometimes very hot and dry biome. Such characteristics of A. cajennense make this tick species specifically adapted to sites under anthropogenic pressure. In this sense the recent concern with preservation might be a double edged sword if not appropriately handled; increase in small forest fragments in both urban and rural areas without the original animal diversity seems to favor A. cajennense ticks and eventually associated tick-borne diseases, a matter of concern for both human and animal health. Acknowledgments The authors would like to thank to Sr. Ze´ do Panga for helping within the reserve. This research was supported by Fundac¸a˜o de Amparo a` Pesquisa do Estado de Minas Gerais—FAPEMIG, Federal University of Uberlaˆndia, Coordenac¸a˜o de Aperfeic¸oamento de Pessoal de Nı´vel Superior—CAPES
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(Doctoral fellowship to V.A.V.) and Conselho Nacional de Desenvolvimento Cientı´fico e Tecnolo´gico— CNPq (Academic Career Research Fellowship to M.P.J.S.).
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