Veterinary Parasitology 161 (2009) 270–275

Population dynamics of Rhipicephalus sanguineus (Latrielle, 1806) inBelo Horizonte, Minas Gerais state, Brazil

Julia A.G. Silveira a, Lygia M.F. Passos a, Mucio F.B. Ribeiro b,*a Escola de Veterinaria, UFMG, CEP 31270-901, Belo Horizonte, MG, Brazilb Departamento de Parasitologia, Instituto de Ciencias Biologicas, UFMG, CEP 31270-901, Belo Horizonte, MG, Brazil

A R T I C L E I N F O

Article history:

Received 31 July 2008

Received in revised form 20 January 2009

Accepted 26 January 2009

Keywords:

Rhipicephalus sanguineus

Population dynamics

Dogs

Belo Horizonte

A B S T R A C T

Rhipicephalus sanguineus ticks are distributed throughout the world, especially in those

areas in which dogs are in close contact with humans. R. sanguineus and fleas are regarded

as the main ectoparasites infesting dogs in Brazil. Besides causing direct damage during

the blood feeding process, this tick species can also transmit pathogens to dogs and

humans. Despite its importance in Brazil, data regarding the seasonality of R. sanguineus

are limited, especially with regard to natural infestations of dogs. The present study aimed

to evaluate the seasonality of R. sanguineus on dogs living in Belo Horizonte, state of Minas

Gerais. From August 2006 to July 2007, ticks were collected monthly from 12 adult dogs in

nine houses, which were located in two districts in the north region of the city. In parallel,

canine clients of a pet care department of the small animal veterinary clinic were

examined for the presence of ticks before bathing and/or clipping. The climatic data

recorded for Belo Horizonte during the experimental period were: mean temperature

18.6 8C; relative air humidity 56.5%; rainfall 37 mm. The only species of ticks identified

from all infested dogs was R. sanguineus, which was found in all its development stages.

Among dogs living in houses, three tick population peaks were observed (August,

February, and June), suggesting the occurrence of three generations per year in Belo

Horizonte. A total of 7318 ticks were collected, of which 5422 were adult ticks and 1896

represented immature stages (744 larvae and 1152 nymphs). The monthly inspection of

dogs living in houses demonstrated significantly higher parasitism during the dry season

(p < 0.05). A total of 2848 dogs from the pet care department of the small animal

veterinary clinic were examined, of which 222 (7.8%) were infested with ticks and the

percentage of infested dogs in the dry season was higher (p < 0.05) than in the hot wet. The

percentage of male dogs infested with ticks was significantly higher (58.29%) than the

percentage of infested female dogs (41.70%). This study of the dynamics of R. sanguineus

infestations in Belo Horizonte will contribute to establishing appropriate measures to

control tick infestations in dogs.

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1. Introduction

Originally from the African continent, the brown dogtick, Rhipicephalus sanguineus (Latrielle, 1806), is distrib-

* Corresponding author. Tel.: +55 31 3409 2842; fax: +55 31 3409 2970.

E-mail address: muciobr@mono.icb.ufmg.br (Mucio F.B. Ribeiro).

0304-4017/$ – see front matter � 2009 Elsevier B.V. All rights reserved.

doi:10.1016/j.vetpar.2009.01.028

uted throughout the world due to the close associationbetween dogs and humans (Walker et al., 2005). Thesecanids are the only hosts of the three tick parasitic stages(larvae, nymphs, and adults), and dogs are an uncondi-tional factor for establishment of the ixodid population(Szabo et al., 1995). The climatic seasons influence theestablishment of non-parasitic stages and the R. sanguineus

biological cycle. Temperatures under 18 8C and relative air

J.A.G. Silveira et al. / Veterinary Parasitology 161 (2009) 270–275 271

humidity (R.H.) under 50% limit the continuity of this cycle(Maroli et al., 1996; Bellato and Daemon, 1997). Non-parasitic stages of R. sanguineus are located near the host’sresting or sleeping place, awaiting the arrival of the animal(Labruna and Pereira, 2001).

Tick infestation rates have been increasing duringrecent decades, and R. sanguineus and fleas are currentlythe most important ectoparasites among dogs in Brazil(Labruna, 2004). Tick parasitism is harmful to dogs and,moreover, R. sanguineus ticks are known vectors ofpathogens such as Babesia canis, which infects dogs(Hoskyns, 1991); Rickettsia rickettsii and R. conori, whichinfects humans (Mariotte et al., 1944; Maroli et al., 1996);and Ehrlichia canis, which infects both hosts (Benenson,1992).

Despite the importance of direct and indirect damagecaused by tick infestations, few studies about the biologyand seasonality of R. sanguineus in Brazil have been carriedout using primarily natural conditions. Only one studyexamining the seasonal dynamics of R. sanguineus wascarried out at a kennel located in a police unit in Goiania,state of Goias, Brazil. The results of this study showed thatixodids can develop up to four generations yearly, and doginfestations were observed throughout the year (Louly,2003). Information is available regarding the seasonaldistribution of R. sanguineus over the course of 3 yearsreported from small animal veterinary clinics in Morelos,Mexico. This information demonstrates 2.5 yearly genera-tions of R. sanguineus, and a positive correlation betweenthe prevalence of ticks and rainfall in the spring, summerand autumn, whereas there was only a correlation withtemperature during the winter (Cruz-Vazquez and Garcia-Vazquez, 1999).

Considering the minimal data regarding the biologicalcycle of R. sanguineus in natural dog infestations, and thatsuch information is essential for the establishment of R.

sanguineus control measures, the present study aimed toevaluate the seasonality of R. sanguineus on dogs living inBelo Horizonte, state of Minas Gerais, Brazil.

2. Materials and methods

All activities in these studies were approved by the localanimal use committee (CETEA/UFMG—Comite de Etica emExperimentacao Animal).

From August 2006 to July 2007, ticks were collectedmonthly from 12 adult dogs (7 males and 5 females) innine houses, which were located in two districts in thenorth region of Belo Horizonte, Minas Gerais. All dogs werenaturally infested with R. sanguineus, and ticks werecollected manually and by brushing the animals. Ixodidswere collected from the left side of the dogs between8:30 a.m. and noon.

Manual collection was utilized when the ticks wereattached to the dog. In order to accomplish this collection,the body of the animal was divided into areas:

� A

rea 1—head and ears; � A rea 2—between the toes (anterior and posterior); � A rea 3—neck, forelegs, armpits, chest, back until the

insertion of the last rib;

� A

rea 4—abdomen, hind legs, groin, tail, and back after theinsertion of the last rib.

Area 5 was designated for the quantification of ticksrepresenting immature stages and non-attached adultsobtained via brushing.

The collected ticks were maintained in tubes containingethanol (70%), and the tubes were identified based on thecollection areas. All collected specimens were identifiedusing a stereoscopic microscope Olympus SZ 40 accordingto Aragao and Fonseca (1961) and Walker et al. (2005).

A questionnaire was developed and applied monthly inorder to verify if the dog owner noted the presence of R.

sanguineus in the environment and on the dog betweencollections. The owners were instructed to note thepresence of ticks on themselves, and they received tubescontaining ethanol (70%) for keeping any ticks that werefound.

R. sanguineus colonies were established in the labora-tory under controlled conditions (24 8C, 80% R.H.) to followthe duration of their biological cycle. In February 2007,eight engorged females collected from dogs were placed ina chamber (B.O.D.) to assess oviposition. After 12 days oflarva hatching, rabbits (Oryctolagus cuniculus) were usedfor larva feeding using a rubber chamber (E.V.A.—etil vinylacetate), which was sealed with cotton fabric fixed in placeusing special glue (BRASCOPLAST1—Brascola LTDA, SaoBernardo do Campo, SP, Brazil). After feeding anddetaching from the host, the engorged larvae were keptinside the chamber until they developed into nymphs. Thenymphs were fed on rabbits until total engorgement. Themoult to adult form occurred in the B.O.D. chamber, and 12days after changing, the specimens were selected based onsex and kept in tubes containing ethanol (70%).

Between August 2006 and July 2007, at the same time ofthe study performed in houses, a study in the pet caredepartment of a small animal veterinary clinic in the sameregion was performed. All canine clients were examinedduring this period for the presence of ticks before bathingand/or clipping by trained employees. A questionnaire wascompleted for each dog containing information such asname, breed, sex, inspection date, and the presence orabsence of ticks.

3. Environmental data

Climatic data for Belo Horizonte were obtained from the5th Meteorological District of the Meteorology NationalInstitute—INMET. Monthly measurements of temperature,relative humidity (R.H.), and total rainfall were obtainedfor the entire study period.

4. Data analysis

In order to calculate the total infestation, the number ofticks obtained per animal and per collected area wasduplicated (Louly, 2003). Analyses were performed usingthe Bioestat and Instat Program according to Sampaio(2004).

The tick infestation means from male and female dogsmonthly followed in houses were analyzed by the Mann–

J.A.G. Silveira et al. / Veterinary Parasitology 161 (2009) 270–275272

Whitney test. The Chi-square test evaluated proportionsbetween male and female ticks and evolutive stages ofticks. Considering the total number of ticks observed ondogs, the infestation rates were analyzed by Wilcoxonmatched-pairs signed-ranks test during distinct seasons:the dry season (autumn and winter) and the hot wetseason (spring and summer) (Sampaio, 2004). The Fried-man test compared body areas of the same dog during thestudy period.

The Chi-square test was used to compare infested andnon-infested dogs inspected in the pet care department ofa small animal veterinary clinic during the differentseasons.

5. Results

Climatic variables, including temperature, R.H., andtotal rainfall during the experimental periods assessed inBelo Horizonte are shown in Fig. 1. The highest tempera-ture was observed in March (29.9 8C) and the lowesttemperatures were observed in June and July (15.7 8C). The

Fig. 1. Climatic data for temperature: minimum, mean, maximum (8C), relative h

Horizonte, state of Minas Gerais, Brazil.

highest R.H. (78%) was observed in January and the lowestwas recorded in May (44%). Total rainfall data showed thatthe highest and lowest values were registered in January(350.9 mm) and June (0.0 mm), respectively.

During the experiment, 7318 ticks were collected, andall ixodids were identified as R. sanguineus. Larvae, nymph,and adult stages were found on dogs during all months ofthe experiment. Considering all the ticks collected duringthe experiment, the occurrence of three infestation peaksdemonstrated the generation number per year (Fig. 2).

No statistically significance was observed consideringthe sex of the dogs (p = 0.3434). So, analysis considered allthe dogs together.

The highest number of collected tick stages was foundin August, and the lowest was found in May. Three peaks oftotal ticks were observed: August 2006, and February 2007and June 2007 and three peaks of adult ticks wereobserved: October 2006, and March and July 2007.Immature stages were distributed in four larva populationpeaks: August and November 2006 and January and April2007. Finally, four nymph population peaks were

umidity (%), and total rainfall (mm) from August 2006 to July 2007 in Belo

Fig. 2. Monthly variations in Rhipicephalus sanguineus larvae, nymph, and

adult populations on dogs from August 2006 to July 2007 in Belo

Horizonte, state of Minas Gerais, Brazil.

Fig. 3. Percentage of collected R. sanguineus per collection area on dogs:

Area 1: head and ears; Area 2: between the toes (anterior and posterior);

Area 3: neck, forelegs, armpits, chest, back until the insertion of the last

rib; Area 4: abdomen, hind legs, groin, tail, and back after the insertion of

the last rib; Area 5: ticks representing immature stages and non-attached

adults collected via brushing. The number of collected ticks from different

areas of the dogs is statistically distinct (p < 0.05) according to the

Friedman test.

Table 1

Percentage of infested dogs during the different seasons inspected in the

pet care department of a small animal veterinary clinic in Belo Horizonte,

state of Minas Gerais, Brazil, from August 2006 to July 2007.

Season Infested/total Infestation rate (%)

Dry (autumn–winter) 134/1496 8.96

Raining (spring–summer) 88/1252 7.03

Total 222/2848 7.8

J.A.G. Silveira et al. / Veterinary Parasitology 161 (2009) 270–275 273

recorded: August 2007 and February, April, and June 2007(Fig. 2).

Considering the total number of ticks observed on dogs,were observed 4928 ticks on the dogs during the dryseason (winter and autumn) and 2390 ticks on the dogsduring the hot wet season (spring and summer). Theinfestation rates were significantly higher during the dryseason (p < 0.05).

A statistically significant higher number of adults thanimmature stages was observed, with a proportion of 2.8:1(p < 0.05). Among the adults, male ticks were statisticallymore frequent than females, 1.1:1 (p < 0.05). The propor-tion of nymphs to larvae was 1.5:1 (p < 0.05). The numberof engorged stages was statistically higher than non-engorged stages for all evolutive stages (p < 0.05).

The most infested area of the animals was Area 3 (neck,forelegs, armpits, chest, back until the insertion of the lastrib) (p < 0.05), where 46.11% of the ticks were collected(Fig. 3).

Dog owners mentioned the presence of ticks on theanimals during the experimental period, but the largestinfestations occurred in October and November. Thepresence of ticks in the environment was observed byresidents in 44.4% of the houses in July, October, andJanuary. However, R. sanguineus infestation of humans wasnot detected in this experiment.

According to the observed parameters of the biologicalcycle of R. sanguineus, which were maintained in controlledconditions by establishment of colonies, the incubationperiod of the eggs was between 32 and 42 days. After 12days of moulting, the larvae were fed on rabbits, followedby engorgement and detachment after 3–4 days. The fedlarvae required a mean of 10 days to moult into nymphs.After 12 days of this moulting, the nymphs were again fedon hosts, followed by detachment after 4–5 days. Moultingto adults required a mean of 15 days. Therefore, the wholebiological cycle from larval moulting to the adult stage wascompleted in 58 days.

During the study in the pet care department of the smallanimal veterinary clinic, 2848 dogs were inspected. Amongthese dogs, 7.8% (222 animals) were infested with ticks.Statistically significance was observed (p = 0.343), show-

ing to these dogs was more infested in the dry season(Table 1).

Of the 222 infested dogs, the males (58.29%) werestatistically (p < 0.05) more affected than females(41.70%). With regard to fur length, 77.87% of the infesteddogs had long fur, which is statistically (p < 0.05) morefrequent than infested dogs with short fur.

6. Discussion

Climatic factors significantly influence the biologicalcycle of R. sanguineus, mainly during the non-parasiticphase. The weather in Minas Gerais is classified as tropical,with alternations of humidity and dryness. It is character-ized as typically warm and semi-humid tropical weather,with a rainy season (spring and summer) and a dry season(autumn and winter) (Strahler, 2007).

In this study, all stages of the biological cycle of R.

sanguineus were found during all periods of the experi-ment; however, there was significant variation (p < 0.05)with regard to infestation rates and seasons. The winterand autumn periods (dry season with a mean temperature18.6 8C, mean R.H. of 56.6%, and mean precipitation of37 mm) demonstrated the highest tick count, although onepeak in immature stages was observed in June, with aprecipitation of 0.0 mm and the lowest temperatureregistered (15.7 8C).

The seasonal variation of R. sanguineus observed in BeloHorizonte differs from the results of studies developed in

J.A.G. Silveira et al. / Veterinary Parasitology 161 (2009) 270–275274

other Brazilian cities. In Goiania, Goias, Louly (2003)demonstrated the presence of ticks during all months ofthe year but did not verify significant difference in countswith regard to the seasons. This could be explained by thefact that the study was developed at kennels that werewashed twice per day, resulting in a stable humidity thatcould interfere with the biological cycle of R. sanguineus. Inthe city of Juiz de Fora, Minas Gerais, Rodrigues et al.(2001) collected ectoparasites from dogs during the winterand summer. Although they did not observe a significantdifference in tick count frequency, it is important to pointout that the dogs included in this study lived in the streetswithout any care.

Maroli et al. (1996) confirmed that R. sanguineus do notdevelop at temperatures lower than 18 8C and R.H. lowerthan 50%. In the present study, the lowest recordedtemperature was 16.6 8C and R.H. was 44% in May 2006;however, we observed cycle continuity, and all tick stageswere found on dogs, although May demonstrated thelowest collected tick counts. The constant presence of thehost throughout the year and suitable environments orthe non-parasitic phases may explain why the climaticvariations were not limiting for the development of R.

sanguineus.The occurrence of three peaks in total ticks collected

suggests that R. sanguineus develops three generations peryear in Belo Horizonte. In this case, the complete cycle ofthis ixodid lasted approximately 121 days. Under con-trolled conditions, the cycle was completed in 58 days. Thistime decrease in the R. sanguineus biological cycle can beexplained because the non-parasitic phases occurred inideal conditions of temperature and R.H. (Sartor et al.,1996).

The generation numbers obtained in the present studydiffer from the data described by Louly (2003) in Goiania,where four peaks were recorded. On the other hand, ourresults were similar to those obtained by Cruz-Vazquezand Garcia-Vazquez (1999) in Mexico, where there were2.5 generations per year. The differences among thestudies are probably related to the local weather or theapplied methodology.

The larger proportion of male compared to female ticksobserved in the present study could be due to the fact thatfemales detached from the host for oviposition, whilemales remained attached for a longer period of time(Yousfi-Monod, 1985).

The results obtained for the area of the dogs exhibitingthe highest infestation are in agreement with Hoskyns(1991), Labruna and Pereira (2001), Rodrigues et al.(2001), Louly (2003), and Labruna (2004). Because R.

sanguineus presents short mouthparts, it tends to attachitself in areas that the dog has difficulty accessing, the skinis not very thick, and the blood irrigation is plentiful(Theis, 1968). According to Labruna and Pereira (2001),the area between the toes is a preferential local for tickfixation.

In the study at the pet care department of the veterinaryclinic, there was a significant difference (p < 0.05) withregard to tick infestations among the observed months.Comparisons between the data obtained from dogsinfested with ticks at the pet care facility and those

infested with adult ticks in houses demonstrated that thedry season has a higher infestation rate.

The lower rate of tick infestation among animalsinspected at the pet care department of the veterinaryclinic could be due to the care provided by the owners,including manual collection of ectoparasites when found.The higher percentage of infested among dogs with longfur could be related to the difficulty associated withmanual collection and reduced visibility of the ticks.Furthermore, animals with long fur have more difficultyremoving the ixodids during scratching, which increasesthe infestation rate.

During the experimental period, tick infestation ofhumans was not detected even though high-infestationrates were observed for dogs, or ticks were observed on thewalls and ceilings of the houses. Although there are manyrecords of ticks on humans in other countries (Felz et al.,1996; Manfredi et al., 1999), there are few papersdescribing R. sanguineus parasitism of humans in Brazil(Dantas-Torres et al., 2006; Louly et al., 2006). The differentlevels of R. sanguineus anthropophily could be due todisagreements regarding the species of genus Rhipicepha-

lus in Brazil (Szabo et al., 2005; Oliveira et al., 2005).In conclusion, Belo Horizonte can be considered as a city

with ideal climatic conditions for the establishment of R.

sanguineus because three generations were observed peryear. The collection of stages, even during less than idealtemperature and R.H. conditions, and the high number ofticks found during the dry season suggest a high rate of R.

sanguineus adaptation in this region when the presence ofthe preferred host is constant in the environment,independent of the use of acaricides by owners in non-controlled conditions.

Acknowledgements

The authors are grateful to CAPES (Coordenacao deAperfeicoamento de Pessoal de Nıvel Superior) for scholar-ships, to FAPEMIG (Fundacao de Amparo a Pesquisa doestado de Minas Gerais), to Schering-Plough and Merial doBrasil Companies for acaricide products at the end of theexperiment, to Recanto Animal Veterinary Clinic, to theresearchers Gustavo F. Paz, Camila V. Bastos and Luciana F.Oliveira. We thank American Journal Experts reviewers forimproving of English writting and for all contributions thatallowed us to execute the present study.

References

Aragao, H., Fonseca, F., 1961. Notas de ixodologia VIII. Lista e chave pararepresentantes da fauna ixodologica brasileira. Mem. Inst. OswaldoCruz 59, 115–129.

Bellato, V., Daemon, E., 1997. Influencia da temperatura de manutencaode fase nao parasitaria sobre a fase parasitaria de Rhipicephalussanguineus (Latreille, 1806) (Acari: Ixodidae). Rev. Bras. Parasitol.Vet. 6, 15–19.

Benenson, A.S. (Ed.), 1992. El control de las enfermedades transmisiblesen el hombre. Organizacion Mundial de Salud, Washington, DC, pp.115–117.

Bioestat Program 4.0. http://www.mamiraua.org.br/noticias.php?cod=3(accessed October 1, 2007).

Cruz-Vazquez, C., Garcia-Vazquez, Z., 1999. Seasonal distribution ofRhipicephalus sanguineus ticks on dogs in urban area of Morelos,Mexico. Exp. Appl. Acarol. 23, 277–280.

J.A.G. Silveira et al. / Veterinary Parasitology 161 (2009) 270–275 275

Dantas-Torres, F., Figueredo, L.A., Brandao Filho, S.P., 2006. Rhipicephalussanguineus (Acari: Ixodidae), the brown dog tick, parasitizing humansin Brazil. Rev. Soc. Bras. Med. Trop. 39, 64–67.

Felz, M.W., Durden, L.A., Oliver Jr., J.H., 1996. Ticks parasitizing humans inGeorgia and South Carolina. J. Parasitol. 82, 505–508.

Hoskyns, J.D., 1991. Tick transmitted diseases. The brown dog tick Rhi-picephalus sanguineus (Latreille, 1806). Vet. Clin. North Am. SmallAnim. Pract. 21, 99–101.

Labruna, M.B., Pereira, M.C., 2001. Carrapatos em caes no Brasil. ClınicaVeterinaria 30, 24–32.

Labruna, M.B., 2004. Biologia e ecologia de Rhipicephalus sanguineus(Acari: Ixodidae). Rev. Bras. Parasitol. Vet. 13 (Suppl. 1), 123–124.

Louly, C.C.B., 2003. Dinamica sazonal de Rhipicephalus sanguineus (ACARI:IXODIDAE) no canil da Polıcia Militar do municıpio de Goiania - Goias,Brasil. Dissertacao (Mestrado) - Faculdade de Medicina Veterinaria daUniversidade Federal de Goias, Goiania, GO.

Louly, C.C.B., Fonseca, N.I., Oliveira, V.F., Borges, L.M.F., 2006. Ocorrencia deRhipicephalus sanguineus em trabalhadores de clınicas veterinarias ecanis,nomunicıpiodeGoiania,GO.CienciaAnimalBrasileira7,103–106.

Manfredi, M.T., Dini, V., Piacenza, S., Genchi, C., 1999. Tick species para-sitizing people in an area endemic for tick-borne diseases in north-western Italy. Parassitologia 41, 555–560.

Mariotte, C.O., Bustamante, M.E., Varela, G., 1944. Hallazgo del Rhipice-phalus sanguineus Latreille infectado naturalmente com fiebre man-chada de las montanas rocosas, em Sonora (Mexico). Rev. Inst. Salub.Enf. Trops. 5, 297–300.

Maroli, M., Khoury, C., Frusteri, L., Manilla, G., 1996. Diffusione della zecadel cane (Rhipicephalus sanguineus Latreille, 1806) in Italia: un pro-blema di salute pubblica. Ann. Inst. Super. Sanita 32, 387–397.

Oliveira, P.R., Bechara, G.H., Denardi, S.E., Saito, K.C., Nunes, E.T., Szabo,M.P.J., Mathias, M.I.C., 2005. Comparison of external morphology ofRhipicephalus sanguineus (Acari: Ixodidae) ticks from Brazil andArgentina. Vet. Parasitol. 129, 139–147.

Prefeitura Municipal de Belo Horizonte. Distritos sanitarios http://por-tal2.pbh.gov.br/pbh/index.html;jsessionid=9ddc33757448ebc11cd-ded07fb9aebf2?id_conteudo=4338&id_nivel1=-1 (accessed July 15,2007).

Rodrigues, A.F.S.F., Daemon, E., D’Agosto, M., 2001. Investigation of someectoparasites from street dogs in the Municipality of Juiz de Fora,Minas Gerais. Rev. Bras. Parasitol. Vet. 10, 13–19.

Sampaio, I.B.M. (Ed.), 2004. Estatıstica aplicada a experimentacao animal.Fundacao de Ensino e Pesquisa em Medicina Veterinaria e Zootecnia,Belo Horizonte, 265 pp.

Sartor, A.A., Cunha, D.W., Daemon, E., 1996. Aspectos da biologia deRhipicephalus sanguineus (Latreille, 1806) (Acari: Ixodidae) emcondicoes de laboratorio: fase parasitaria de larvas, ninfas efemeas e nao parasitarias de larvas e ninfas. Rev. Bras. Med.Vet. 18, 14–17.

Strahler, A. Climas que ocorrem no Brasil. http://www.coladaweb.com/geografia/climas_brasil.htm (accessed September 10, 2007).

Szabo, M.P.J., Mukai, L.S., Rosa, P.C.S., 1995. Differences in the acquiredresistance of dogs, hamsters, and guinea pigs to repeated infestationswith adult ticks Rhipicephalus sanguineus (Acari: Ixodidae). Braz. J.Vet. Res. Anim. Sci. 32, 43–50.

Szabo, M.P.J., Mangold, A.J., Joao, C.F., Bechara, J.H., Guglielmone, A.A.,2005. Biological and DNA evidence of two dissimilar populations ofthe Rhipicephalus sanguineus tick group (Acari: Ixodidae) in SouthAmerica. Vet. Parasitol. 130, 131–140.

Theis, J.H., 1968. Mechanical removal of Rhipicephalus sanguineus from thedog. J. Am. Vet. Med. Assoc. 153, 433–437.

Walker, J.B., Keirans, J.E., Horak, I.G. (Eds.), 2005. The Genus Rhipicephalus(Acari: Ixodidae): A Guide to the Brown Ticks of the World. CambridgeUniversity Press, Cambridge, p. 643 pp..

Yousfi-Monod, R., 1985. Evolution annuelle de la sex ratio de Rhipicepha-lus sanguineus (Acarina, Ixodidae) en zone urbaine de l’ouest Algerien.Acarology 26, 361–365.