Hair sheep breeds are a new, cost-effective option for the diversification of livestock in the Midwest region of Brazil. They are grazed extensively with cattle as well as in isolation in small areas. Hair sheep breeds are ulnerable to infestation by parasites such as the cattle tick, Rhipicephalus microplus, which causes various types of damage and can transmit diseases

AGUIRRE, A. de A. R.

ANDREOTTI, R.

BARROS, J. C.

GARCIA, M. V.

KOLLER, W. W.

MATIAS, J.

REIS, F. A.

English

Repository Open Access to Scientific Information from Embrapa

Garcia et al. Parasites & Vectors 2014, 7:515http://www.parasitesandvectors.com/content/7/1/515RESEARCH Open AccessContributions of the hair sheep breed Santa Inesas a maintenance host for Rhipicephalus(Boophilus) microplus (Acari: Ixodidae) in BrazilMarcos Valério Garcia1, Renato Andreotti1*, Fernando Alvarenga Reis2, André de Abreu Rangel Aguirre3,Jacqueline Cavalcante Barros1, Jaqueline Matias3 and Wilson Werner Koller1AbstractBackground: Hair sheep breeds are a new, cost-effective option for the diversification of livestock in the Midwestregion of Brazil. They are grazed extensively with cattle as well as in isolation in small areas. Hair sheep breeds arevulnerable to infestation by parasites such as the cattle tick, Rhipicephalus microplus, which causes various types ofdamage and can transmit diseases.Methods: In this study, Santa Inês hair sheep were naturally infested in an area contaminated by infested cattleand then monitored to determine the ability of these animals to maintain the local tick population in the absenceof cattle. After engorged tick females of each generation fell off, the animals were placed in another pasture andwere returned only after larvae reappeared in the original pasture.Results: Tick counts were performed every ten days for three generations of sheep, and average infestations peranimal of 34, 12 and 4 ticks were observed for each successive generation. These numbers suggest the acquisitionof resistance; however, additional studies are needed to ensure resistance is achieved. The average length of theparasitic phase for each generation of ticks was 25 days.Conclusion: We concluded that this hair sheep breed, even if kept separate from cattle, is able to maintain tickpopulations for at least three generations, although a gradual decrease in the population levels of R. microplusover three generations was observed. We also detected two positive cases of Anaplasma spp. Therefore, itappears that the Santa Inês hair sheep breed contributes to the circulation of this bacterium among otherruminants.Keywords: Rhipicephalus microplus, Santa Ines hair sheep, Pastures, Biological cycle, BrazilBackgroundThe Santa Inês hair sheep breed is originally from thenortheastern region of Brazil, and is popular in theBrazilian Midwest for breeding to produce lambs formeat production because the weather in this region isfavorable for this industry [1]. In areas with moreextensive livestock production in the savanna, grazingof sheep with beef cattle is common [2], but may createhealth complications for both species [3]. The cattle tickRhipicephalus (Boophilus) microplus and the diseases that* Correspondence: renato.andreotti@embrapa.br1Molecular Biology Laboratory, Embrapa Beef Cattle, Campo Grande, MS,BrazilFull list of author information is available at the end of the article© 2014 Garcia et al.; licensee BioMed Central LCommons Attribution License (http://creativecreproduction in any medium, provided the orDedication waiver (http://creativecommons.orunless otherwise stated.this tick can transmit contribute to such health problems.This parasite is considered responsible for notable eco-nomic losses in livestock holdings [4], therefore its controldeserves special attention.The occurrence of ticks of the genus Rhipicephalus,among others, in sheep has been widely reported inBrazil and other countries [5-13]. In Brazil, specificstudies have largely been restricted to the sheep indus-try in the northeastern region due to the traditionalbreeding of hair sheep that are able to withstand thelocal climatic conditions. In the southern region, wherethe weather is temperate, production of wool and furrepresents additional gains because wool-producing breedsare preferred.td. This is an Open Access article distributed under the terms of the Creativeommons.org/licenses/by/4.0), which permits unrestricted use, distribution, andiginal work is properly credited. The Creative Commons Public Domaing/publicdomain/zero/1.0/) applies to the data made available in this article,Garcia et al. Parasites & Vectors 2014, 7:515 Page 2 of 4http://www.parasitesandvectors.com/content/7/1/515The occurrence of ticks, particularly R. microplus, inhair sheep breed species is of increasing concern due tothe rapid expansion of the sheep industry into new areastraditionally used only for cattle and horses, as observedin the State of Mato Grosso do Sul.Considering the risk of R. microplus infestation whensharing pastures or from neighboring pastures, the presentstudy evaluated the ability of the hair sheep breed tomaintain parasite populations after the withdrawal of thebovines as the tick source.MethodsStudy area and animals usedThe observations were conducted in an experimentalfield on the Embrapa Beef Cattle farm, Campo Grande,MS, at the coordinates 20.448779 S and 54.713643 W.Temperature and rainfall data were obtained from aclimatological station located at an approximate altitudeof 530 meters and coordinates 20° 27’ S and 54° 37’ W.According to the Köppen & Geiger [14] classification, thearea of this study lies in the transition between the Cfahumid climate, without a dry season, and the tropicalhumid AW climate, with a rainy season in summer and adry season in winter.Two paddocks were utilized, each of which had anarea of 0.5 ha containing Brachiaria decumbens.Paddock A was infested with Rhipicephalus microplus,and the proximal paddock B was free of ticks. Cattleinfested with R. microplus previously occupied paddockA for a period of four days (February 21 to February 24of 2013). After the withdrawal of these bovines, ninepregnant Santa Inês sheep were placed in the same pas-ture. After 41 days, the sheep were naturally infested byticks. This study addresses the monitoring of the naturalinfestation of these sheep by ticks. The observed num-ber of sheep increased to 14 over the course of the mon-itoring period due to the birth of five lambs in the initialgroup.Pasture examinations for the presence of tick larvaeBetween and during all tick generations, the pasture wasmonitored weekly by three people to observe the presenceof larvae on the top of the grass leaves. For each tickgeneration, the pastures were monitored from the earlyappearance of larvae in the grass until their completedisappearance, when that generation, including the re-spective parasite cycle, was reported as complete.Sheep examinations for ticks and handling of animalsbetween paddocksThe sheep were examined daily to register the presenceof larvae and the accompanying development of ticksand determine tick detachment by counting the remainingspecimens. The parasitic period comprised the time fromthe detection of the first larvae on the sheep to the detach-ment of engorged females.When the parasitic phase was complete, the animalswere removed to a nearby pasture (paddock B) to avoidpossible overlapping tick generations. When larvae ap-peared in paddock A, the sheep were brought back andremained through the development and completion ofthe parasitic phase of the new tick generation. Then, thepasture transfer process was repeated. When the firstlarvae were again detected on the grass, the sheep werereturned to paddock A for observation of the next para-sitic cycle. The lambs were kept with the initial group andwere subjected to the same evaluation system.Infection with Babesia and AnaplasmaBlood was collected from the animals for a blood smeartest and for serology to identify the presence of Babesiaand Anaplasma. A sample of 3 mL per animal was takenonce during each parasite period, and the samples wereplaced into tubes containing sodium citrate (1 part citrateat 104 nmol/L plus 9 parts blood) for DNA extraction.A 100-μl aliquot of blood was used to extract DNAusing a DNAzol kit Invitrogen® (Carlsbard, US A) accord-ing to the manufacturer's recommendations. Polymerasechain reaction (PCR) for Babesia spp. was performedusing the primers KB-16 and KB-17, while the primers,Ana-F and Ana-R were used to detect Anaplasma spp.[15,16]. The resulting PCR products were separated byelectrophoresis on a 1.5% agarose gel with ethidium brom-ide staining.Results and discussionTick-infested sheep were identified on April 4, 2013;based on tick size, the ticks were estimated to be ap-proximately six days into the parasitic cycle. Thus, therewas an estimated interval of 33 days between the removalof the cattle and early infestation (February 24 to March29, 2013). This estimate was based on the average tickincubation period of 28 days [17], determined underenvironmental conditions similar to those present duringthe development of the observed first cycle.The second generation began after the 48th day, asmeasured from the fall of the last engorged female tothe appearance of larvae in the pasture (April 10 to May28, 2013). The initial nine sheep and five lambs werereturned to paddock A to be infested again on June 6,2013, and new parasitism was observed beginning onJune 11, 2013. This longer incubation period may haveresulted from the presence of lower temperatures, whichare common in the region during autumn.The third generation began after the 84th day, as mea-sured from the fall of the last engorged ticks from thesheep (July 4 to September 28, 2013). The incubationperiod was thus even longer in the winter due to lowFigure 1 Average number of ticks per animal resulting fromthe natural infestation of a Santa Ines hair sheep breedmaintained in Brachiaria decumbens pastures without cattle forthree periods of infestation. The climatological data for CampoGrande, MS, from February to November 2013 are also shown. As anexample, F1, F2, and F3 represent the ten-day intervals betweenobservations during the month of February and so on for eachindicated month. T = temperature; RH = relative humidity;Acc. = Rainfall (total for the period); and ticks = average numberof individuals per animal.Garcia et al. Parasites & Vectors 2014, 7:515 Page 3 of 4http://www.parasitesandvectors.com/content/7/1/515temperatures than in the previous period. The sheepwere returned to paddock A to be infested again on May10, 2013, in the spring, and parasitism was observed be-ginning on October 26, 2013.Based on the above information, we concluded thatthe hair sheep breed can be parasitized by R. micro-plus, and that the sheep can maintain infested areasand become infested again for at least three successivegenerations.The average number of ticks on the animals was re-corded every ten days during each of the three observedgenerations, and these data are presented in Figure 1.We found that the parasitic phase in each generationlasted an average of 25 days and that the populationpeaks gradually diminished. While the average infest-ation per animal in the first generation was 34 ticks, thisnumber decreased to an average of 12 in the secondgeneration and 4 in the third generation.The climatic data presented in Figure 1 show thatrainfall immediately preceded the beginning of eachparasitic period for the three observed generations,and a total absence of rainfall occurred from the mid-dle of June until the end of August. The dry period ofthe year for the studied region extended from mid-Mayto September. The average temperature during thesecond generation was slightly lower than that duringthe first generation, and the prolonged incubationperiod and beginning of infestation that marked thebeginning of the third generation were attributed tothe occurrence of the lowest average temperatures inthis period.The parasitic phase of the second observed generationdeveloped in the absence of rain. Thus, drought-relatedeffects likely contributed to the decreased survival rateof the eggs and/or larvae, which was reflected in the lowpopulation levels observed in the third generation. Fromthis study, we can infer that sheep play a role in themaintenance of R. microplus, and that ticks can be main-tained for at least three generations (9 months) in theabsence of cattle.Blood smear tests did not detect presence of Anaplasmaspp. or Babesia spp. However, PCR analysis of a lamb con-firmed the presence of Anaplasma spp. PCR performedon blood from the lamb's mother did not confirm verticaltransmission, suggesting that the infection was transmit-ted by a tick or by some other means. In a previous studyof sheep in the semi-arid region of Brazil, 16-17% ofthe analyzed samples were positive for antibodies toAnaplasma spp., suggesting that species of this genusmay infect small ruminants [18] and such an infectionmay have occurred at the study location.ConclusionSanta Inês sheep are sensitive to natural infestation bythe cattle tick Rhipicephalus microplus and are able tomaintain a tick population in the pasture for at least threegenerations. There was a gradual decrease in the popula-tion levels of R. microplus over the three generationsobserved.Competing interestsThe authors declare that they have no competing interests.Authors’ contributionsMVG and RA conceived and designed the study; JCB, JM, and AARAcollected data; FAR and WWK analyzed the data; MVG, RA, FAR and WWKwrote the manuscript. All authors read and approved the final version of themanuscript.AcknowledgmentsThe research was supported by Coordination for the Improvement of HigherLevel Personnel (CAPES), National Council for Scientific and TechnologicalDevelopment (CNPq) and Embrapa Beef Cattle.Author details1Molecular Biology Laboratory, Embrapa Beef Cattle, Campo Grande, MS,Brazil. 2Embrapa Goats and Sheeps, Sobral, CE, Brazil. 3Graduate Program ofInfectious and Parasitic Diseases, School of Medicine, Universidade Federalde Mato Grosso do Sul (UFMS), Campo Grande, MS, Brazil.Received: 19 June 2014 Accepted: 1 November 2014References1. Quesada M, McManus C, Couto FAD: Efeitos genéticos e fenotípicos sobrecaracterísticas de produção e reprodução de ovinos deslanados noDistrito Federal. Rev Bras Zootec 2002, 31:342–349.2. Carvalho PC, De F, Santos DT, Barbosa CMP, Lubisco DS, Lang CR:Otimizando o uso da Pastagem pela Integração de Ovinos e Bovinos. InAnais do ZOOTEC 2005. Campo Grande: Embrapa Caprinos e Ovinos (CNPC);2005:1–30.Garcia et al. Parasites & Vectors 2014, 7:515 Page 4 of 4http://www.parasitesandvectors.com/content/7/1/5153. Rocha RA, Bresciani KDS, Barros TFM, Fernandes LH, Silva MB, Amarante AFT:Sheep and cattle grazing alternately: nematode parasitism and pasturedecontamination. Small Rumin Res 2008, 75:135–143.4. Grisi L, Leite RC, Martins JRS, Barros ATM, Andreotti R, Cançado PHD, LeónAAP, Pereira JB, Villela HS: Reassessment of the potential economicimpact of cattle parasites in Brazil. Rev Bras Parasitol Vet 2014, 23:150–156.5. Yeruham I, Hadani A, Galker F, Rosen S: The seasonal occurrence of ticks(Acari: Ixodidae) on sheep and in the field in the Judean area of Israel.Exp Appl Acarol 1996, 20:47–56.6. Madeira NG, Amarante AFT, Padovani CR: Diversity of ectoparasites insheep flocks in São Paulo, Brazil. Trop Anim Health Prod 2000, 32:225–232.7. 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Santarém VA, Sartor IF: Fase de vida livre e flutuação sazonal do Boophilusmicroplus em Botucatu, São Paulo, Brasil. Semina Ciencias Agric 2003,24:11–20.18. Ramos RAN, Ramos CAN, Araújo FR, Melo ESP, Tembue AASM, FaustinoMAG, Alves LC, Rosinha GMS, Elisei C, Soares CO: Detecção de anticorpospara Anaplasma sp. em pequenos ruminantes no semiárido do estadode Pernambuco, Brasil. Rev Bras Parasitol Vet 2008, 17:115–117.doi:10.1186/s13071-014-0515-5Cite this article as: Garcia et al.: Contributions of the hair sheep breedSanta Ines as a maintenance host for Rhipicephalus (Boophilus) microplus(Acari: Ixodidae) in Brazil. 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Contributions of the hair sheep breed Santa Ines as a maintenance host for Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in Brazil.

Hair sheep breeds are a new, cost-effective option for the diversification of livestock in the Midwest region of Brazil. They are grazed extensively with cattle as well as in isolation in small areas. Hair sheep breeds are ulnerable to infestation by parasites such as the cattle tick, Rhipicephalus microplus, which causes various types of damage and can transmit diseases.Made available in DSpace on 2018-02-22T00:42:17Z (GMT). No. of bitstreams: 1
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Contributions of the hair sheep breed Santa Ines as a maintenance host for Rhipicephalus (Boophilus) microplus (Acari: Ixodidae) in Brazil.

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