Levels of natural resistance to Boophilus microplus (Acari: Ixodidae) in Carora breed bulls

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(1); Rev. 8iol. Trop., .. '". ,. 46(�):��l1P�,M9l! ". ". ,,. ». :,:';:�\>\,,(i,. Lé"els ofnatural resistance to Boophilus rfticropluS ;(Acilri: �odidae) in Carora breed buUs ". 1. Roy D.Melénde2;l,.r\Jfr�dp C;pt:.onad.ol, Franklin Mujical; Ftal1c.o Cerutti2 an<l Ortelio M.osqll�ra3 I Univérsidal.l CentrOécideÍlta} "ps;m!ito AIvarado", Déc<U1ato de Cienf:¡ias Veterinarias, Apartado postal 66$, BÍ!lquisjmeto� . . Lafa, 300l-A. Venezuéla. FaX:'�8g1 '425989;'�-máil: nne1ende�d�lfÓS.u�ta:é�h:ve " '. í 3. (',. ". Universitáde Mi1anc¡, F�coltá':4i Me¡Ji:clna Veterinaria. Milan. Italy. Ministerio de Agriculturá'Y cria .'(�C). Se�cio Autónomo. de SimidadAhilnal del Estado Lara.(SA�A). Venezuela.. ". .. '. :Qárqq'fsilÍle!q.. ". ;,.;; ·.· '" Jíi"ks,1;��·' P�#�N!(},ophtiP;�Aitt�tRl'lus V; ,�p�estrini"· :�88�i,·'ate . the. m.ost ilJlp.ottant. r7,;�\)¡�� at�ites"�fi,c.itt1�,in th� tFopi�s atids�b-., .. ' �íI>p .. "regions,. tÍot,oñ'lyd�t9the,Wect dam-. . �@·�tte�.ar;thr<1pods,caus,�,�ri!cattIé�;her4s,>b\Jt. álso.1l!fot'the ttans'fItissi.o6::'!ot., dise��s supij¡as balfésip sis, .an��i� p, sisj, ileriQsis �4 , dri,osí�J��,thls ,c�ritmy�ti�¡¿ ��fi�61 'bas" been. ,maiij[�yc�!tjout�YWb�mic�i��thods apply " e ,aCari�i�es.()n; pti,I;�itiz�:,cattle.' ing ' Non . ,éss.",ij.Ck;.:;�otitr�J?:by1i¿�emicals is , ��pensive. t'Ür �' eJlvir�n'f1'l�ti,'tfieyatioften.deiected in. �. �. ��. .. Cci. á1ºst.�fj��se;Q��¡désareJhat1rifu1r. '. '. �. _,J,!."': :"'J,. ':��-,. i '" '. ;. ,.. ,>'�:". ". .. &. '. ;'. ,. ,,'. ,. '. ., •. .','�, :.":':L. mük.�dW�l�f�tetf:�li�¡:·,Wld!ru.exc�",. and é�pñiiQ�:lt�:'has: le�r�';the, cl�velqp;¡7 ment;li)��,;��k,.it:��táiceto tñeseÓhe�nIs'. , . siw ... ,'(1'iíií1�z tin�At!>·. .". ,'." ,' .. " J�8:t};Field rep.oriS: fr.om allig.on{: . ib��tlg tilat tj€;k.resistance te, a�� .'. ;t:icideS isi,,��rigl�.I��easing, .ther��()�e¡i�' 'i, :,' m ve .of cl1�cal./contr()1 i$i';[l� "Jl.'. :main Qbjec. 'ac�e,,�d,j1)l' tlle __�p&�s lior'in Quret�egi�As. . .(SoWtnqn:l9.g�lRblil&hi993);'Iit'yei'tezuela"the .. ' tionis·also sillÚlar: aI} d er'acllfÍd4f treatmenfS are:'weIl 'd.ocuinented, (C.orQ)la4<F: & Milj,tea ·;Í9��)' Thus, other e1ifeCtive,.rií�Ó'ds· in 'tick'. :;�aricidéf�sis�. '. ..,.... :it4�r¡llleq,tic Iailures".· '�;". .".

(2) 692. REVISTA DE BIOLOGlA TROPICAL. control must be used if we want to fight suc cessfully against these ectoparasites, and simul taneously to keep an acceptable level of milk andJor meat production in the tropics. One of these methods is the use of breeds of cattle which are either totally resistant or have sorne degree of resistance to ticks (Frisch 1981, FAO 1990). First aUempts to evaluate natural resistance of cattle against B. microplus were made in Brazil (Villares 1941), using Bos indicus catde to promote resistance against B. microplus. Later studies showed that cattle resistance to ticks was due to the mounting of a protective immune response against ticks by bovine hosts, and this response was heritable for the cattle progeny (Roberts 1968, Roberts & Kerr 1976). In addition, it ís well known that resistance to B. microplus varies, not only between individual bovínes, but also from breed to breed, even in B. indicus (Zebu cattle) as in Bos taurus (European cattle) herds (Francís & Little 1964, Roberts 1968). In general, pure or cross-bred Zebu cattle is worldwide acknowledged as more resistant to B. microplus and other ticks than European cattle (B. taurus). The methodology for studying the levels of host resistance to ixo did ticks is well known (Wharton & Norris 1980, Wíkel 1996). Bríefly, host natural or acquíred resistance to ticks by a cattle breed is deterrnined after assessing several tíck's feed ing and fertility parameters, i.e., reduced engorgment weight, length of feeding period, reduction of tick egg production, reduced per centage of egg hatching, and egg and larvae mortality (Wikel 1996). The application of this methodology and later the genetic selection of those tick resistant cattle led in several coun tries, i.e. Australia, Brazil and sorne regions in Africa, to develop tick-resistant cattle breeds after cross-breeding B. taurus x B. indicus. Among these cattle breeds developed in the tropics are the Sahiwal, Belmont Red, Bradford, Bonsmara, N'Dama and Boran (De Castro & Newson 1993). Australia has been the most suc cessful country in raising breeds of tick-resis tant cattle wÍth significant productivity and with high adaptability to the tropical environment. In. Australia tms success is mainly due to the deep knowledge they have on ecology and popula tion dynamics of ticks and because in this con tinental ísland the individual cattle resistance to ticks has been quantified (Wharton & Norris 1980, De Castro & Newson 1993). In Venezuela, Lara State, Carora regíon, a tropicalized dairy breed is in the process of developement since 1920 which has been named Carora, and it was official1y accepted as a breed in 1989 by the Venezuelan Agriculture and Husbandry Ministry. This breed is the prod uct of empirical genetic crosses among Brown Swiss cattle, indigenous Creole bovines, and Bos indicus in a minor degree (Herrera 1960, Meléndez & ForJano 1'996). The Carora breed cattle shows an average milk yield /cow, per day, of 12 Its., and it shows sorne levels of resis tance to tropical diseases (Herrera 1960). In 1993 a preliminary assay was conducted in order to evaluate the leveIs of tick resistance by Carora breed heifers and cows naturally infected with B. microplus. We found a B. microplus reproductive index (RI) of 38.16% for Carora cattle whereas Holsteín cows showed a RI of 45.48% (Ceruttí et al. 1995). As a con tinuatíon of this previous assay this work was undertaken wíth the maín objective of assessing the Jevels of natural resistance to B. microplus in seven (7) tick-naíve cross-bred Carora bulls (CCB) which were experimentally ínfected with larvae of this tick.. MATERIALS AND METHODS Experimental animals: Seven (7) CCB with mean age of 31 months (range: 26 45 months) were used in order to evaluate the degree of natural resistance in this tropicalized breed against B. microplus. These bulls had been kept in boxes from birth to adult without contact with ticks, thus we considered them as tick-naive bovines. When the experiment start ed bulls were located in boxes at the Carora Artificial Insemination Center (ClAC) since they had been genetically selected as semen donors for an Al programo Bulls had a mean -.

(3) MELEN DEZ et al.:. Leve1s of l1atural resistance lo BoophiluS microplus. of 623 Kg(range: 538-774 Kg) at the beginning ofthis trial, and they had received alast mosquicide treatment 35 days ago.Bulls body weight. were housed in individual roofed boxes and. body temperature was dailychecked dur the whole biological . eycle of the tick (21. 693. The fourrecorcled para by theír llleans eX)' vari. Statistical analysis:. metets were described. eijor.. ance .and standard. Next,.a multiple com. parative study oftheir variances wasconducted. their. and the significant differences detected Were. ing. analyzed. n. days). In addition, one insecticide. was applied. at ClAC during this period and movement of .. other bovines was 6ght controled. Tick inf��tation: The experimental group of bulls was infested with B. microplus larvae, "Mozo" strain, whieh was kindly supplied by Dr. A. Nari, Instituto Miguel Rubino, Montevideo, Uruguay. This strain has been kept at our laboratory through passages in ticj<-sus. ceptiblecalves. Each buH was infested. with a. mean inoeulum of 6 477 larvae which were 21 old for the time tÍeks were applied along the dorsallineóf eaeh bovine. Seventeen (17) days postinfestation (PI) partialIy fed female B. microplus were counted on eaeh bul!; the process ofcounting was performed only �>n the day. �ight s¡d� ofeach. bovine fol1üwing. teeh.nique.(O'Kelly & Seifert. a. . kn(j;Wn. . 196?). Later,. ()n days21, 22 and 23PI all adult engorgedfem<tle (EF) B. microplus Wllscolleeted fro.l11 tfi�ir h ()sts (tick stanqard lenght. used: 4.5 . - 8.0 I11W) . . arid brought t()'t,helaroratoiy faciHties: ..•... .. .'. ln�u��tion 0fB' 1tlicT?plus: Eachcolle6t-. {�d tick )Vª�counted, w�terwashe? � dried and. we��hted, next.a nindomsawple.. (1.6%.T '3�:�o/é)oj tbese ticks (TabIe . 2) were adhereci at maskil1gtápe andplac#I itl�id�. an i{l(;ub�tor át 27°é:t 1°C an4 90% relative hÚll)ídity,CRH) (Dal g1 iesh � .. Stewatt 198f).At th�epdQf the.· ovipositionperiod (eggs with an oil/ ana s� innirigsheJIplus an áinber coloÍlÍ') was con�cted,weight� 4 al1dfplaceci in vials sealed . with cott()p plugs.Vials were pro�erly identifiéd andp!aced inside the incu bator .until the processof larvaehatching ocurred. A total of four (4) p arameters related to. tick's .. feeding .. ande fel'tility were recorded :and later statistically analYzed. These par�me ters were: adult female tickJ:>ody weight (BW), (RI::;. Dunnett'.s. test. (SAS:. Fe vs Ft (p< 0.0001).. RESULTS Tick parameters:. Boophilus microp lus larvae. completed their lifeeycle in aH infested buIls after. 21 ± 2 days PI and no clínica! signsof tíek�bome in these bovinesdyripg the evaluation>period (mean. réctal1emperature: 385°C; range: 38.0°C - 39.6°C). Thepopulation ofpartia!ly fed female B. micrQplus. counted on . day 17.f>1 oneaqh bull showedgreatvariations (range:63,�670 ticks) (l'ablel).1'hesizeof each laryae in()eul�mapplied to e<!ch.bovine. plus the per¡;;ef\tlge of�FQ. microplllsrecovered arealso shown in TabIe l(Note: intables l and2each row ofdata belongs to eacn indiyidualbtill). diseases wete seen. f..arVlIeinoculul11 appUedperblfll, NO ofj1artially fed JemglfcB. mü:rrpb.lS coanteq ondo.y17PI..and %ofEF B. . micrQplu8 recoverer:ifiorn i'ffested . ctoss�b;edcarJrq�¡'¡lls. .. TicK5 co\mted. · onday 17 PI 6150.. 6315. 6600 6075 7450 7387 5300. 502 670 652 113 290 6� 373. ,:28,1,5 3:43. i&76. 42:03. 39.63 15.57 32.64. Rows: ilÍdividualblllls PI: . post infestation EF: engor�ed females. egg hatching rate. (%EH), ardthe reproduCíive index (RI). EWfBWx%EH).. pare. eacp.norma1 egg!11�ss. é�g . mass weight (EW),. the. using. Statistical Analysis System) which ledto com. in. A total of3(j7EPB. mícroplus were placed incubation, t11ese tícks.had.a: mean 13)\' 01'.

(4) 694. REVISTA DE BIOLOGIA TROPICAL. 213.1 mg (range: 179 - 233 mg) (Table 2), and their pre-oviposition period variedbetween 2 to 4 days. After 2 weeks of oviposition egg masses were weighted and variations were detected in this parameter (Table 2). T he embrionary period lasted 28 days without noticeable changes. The mean %EH was cal culated after stereomicroscopic countings of a mixture of hatched larvae plus unhatched eggs from each EF incubated tick, and this parameter ranged from 14% to 50% (Table 2). Due to these evident varíations in the %EH, the RI for each EF group of ticks also showed significant variations among the 7 bulls (Table 2). Resistance of CCB to ticks: T he compar ative analysis of variances of BW, EW, %EH and RI of collected EF B. microplus showed significant differences (p < 0.001) between the means of these parameters. Nevertheless, when the Dunnett's test was applied, signifi cant differences (Dunnett p <0.05) were only shown between the mean BW of ticks collect ed from bulls 2 and 3. In addition, no signifi cant differences (Dunnett p > 0.05) were detected for the mean BW of ticks from other bulls (Table 2). Applying the same test, signif icant differences (Dunnett p< 0.05) were observed for the parameter EW of ticks col lected from bulls 2, 3, and 7, whereas only for bulls 3 and 6 were detected significant differ ences (Dunnett p< 0.05) for the parameter %EH (Table 2). Finally, the RI only showed significant differences (Dunnett p< 0.05) for bulls 3 and 6 (Table 2). In summary, CCB 3 showed the highest level of resistance since it yielded EF ticks with the lowest mean BW, therefore its EF B. microplus laid minor egg masses, with the lowest %EH (14%) and the lowest ro (7.4) (Table 2). In con trast, bulls 2, 6 and 7 showed a medium level of resistance whereas the other three bulls were considered as non-resistant on the basis of com paring their studied tick parameters against those of bull 3.. TABLE2. Parameters related to B. microplL/s feeding and fertility after ticks completed ¡heir life cyc/e in seven cross-bred Carora BL/lIs. Total EF. XBW. XEW. incubated (n=307). (rng). (rng). %EH. RI. 82. 230. 115. 44. 24.0. 22. 182*. 97*. 44. 26.0. 29. 179*. 72*. 14*. 7.4*. 41. 231. 123. x50. 28.0. 49. 220. 106. 47. 23.0. 50. 233. 112. 28*. 14.0*. 34. 217. 99*. 41. 19.0. *Significant difference(Dunnett p<0.05 ) Rows: individual bulls. EW: egg rnass weight. EF: engorged fernales. %EH: egg hatching rate. BW: tick body weight. RI: reproductive index. DISCUSSION This study has shown that CCB experimen tally infested with B. microplus showed great variability in their natural resistance to tbis tick, thus one bull out of seven was statistical1y detected as tick-resistant after experimentally infested, three were non-resistant, and three showed moderate tick-resistant. This resistance was evaluated in the lab after a multiple com parative analysis of four EF B. microplus para meters. As it is weU known resistance to B. microplus varíes between individual cattle, from breed to breed, and among species of cat tIe. i.e., Bos indicus is more resistant to ticks than B. taurus (De Castro & Newson 1993). These statements are in agreement with the finding that the character "tick resistance" is inheritable by cattle offspring almost in direct proportion to the percentage of Zebu cattJe pre sent in the dam or sire (Arteche 1987). Besides, this character is rather easy to detect and mea sure in the lab sínce the genetic composition of bovine hosts has a strong influence on the life cycle of B. microplus or other ticks (Barriga et al. 1993). On the basis of our results, we con sider that tbis "strong influence" was detected and evaluated in CCB due to its genetic origino.

(5) MELENDEZ et al.: Levels.ofnaturru resistancetoBoophilus.microplus. breed cattle is the·product of genetic amOng Creole cattIe, Bos taurus, and Bos indicus cattJe, consequentIy any Carora Carora. crosses. bovine classified astic.k�resistant should have a. of B. indicus genes, those classified as mOderate tick-resistant shouId probablyhave an eveTi proportion of B. indicus and B. taurus genes; and finalIy those consid ered as non4ick�Tesistant·· should have a· pre" dominance of B. taurusgenes. The great variabilitydetected for B. microplus greater proportion. resistance in CCB is important in particular in a. tropical breed iTi the process ofgenétic consolida. field technicians should startgenetic prograrns selecting Carora heifers and bulls, not only on the basis of pheno type, milk production and breeding data, but aIso tion, since cattle owners and. includingthe factor levels of resistance to B.. microplus.. .. be stated that the character tick resistance must be included in a genetic prograrn of cattle breeding because it meetsthese 4 basic conditions: I)it has a high genetic variability, 2) it is inheritable, 3) it is eCO nomically important and 4) itisrather easy to cal culate. The Jevels of B. mü:roplus resistance '.Vere evaluatedthro4ghJoúfparameters relatedtb f:ed ing �md fertility ofthis tick, and no),"elying only on the EF tick burdens as jt is oftentested and recently questioned (Barriga et al. 1995). FÍIlally, we believethat an effectiveprograrnof tltkcon troJ in the tropícs can be acc01llplished onIy using the basic principIes of integrated. pest manage mení, and in particular using tick-resistant catde. In general, it can. .. 695. contra las' garrapatas en ArnéricaLatina, Infonne· Final.. Consulta de expertos sobtúrradicación de garrapatas. con especial referencia a América Latina. FAn México,12 p.. Barriga, 0., A. Dl\,Silva & J. Azévedo. 1993.lnhibition and recovel)' oC tick functions in cattle repealeadly infested with BoOphilus ínicroplus. 1. Patasitol. 79: 710-715.. Barriga,O., A. Da Silva & J. Azevedo. 1995. Relationships. rO{J¡!l,5C;haracter�. and illtluencesbetween Boophilus mic. .. istics in tick-naive oc repeatedly infested cattle. Ve!.. Parasitol. 56: 225-238.. Cerutti, F., R. Rizzi, R.· D. Meléndez& A;Cotonado. 1995.. Resistenza a Boophilus microplus nella razza bovina Carora.. XI. Congresso. Nazionale. Associazione. Scientifica ¡ji Produzione Anirnale (ASPA). Grado,. Gprizia,Italy. 2 p. Coronado,A . . &F Mujica. 1997. Resistencia a acaricidas en Boophilus microplusen Venezuela. Gac. Cien. Ve!.. 3: 5-13.. Dalgliesh. R. J. & N. P. Stewart. 1982. Sorne effects oftime, ten:¡perature and feeding on infection rates with Babesia. bovisand Babesia bigemina in [joophilus microplus lar. vae., In!. 1. Parasitol. 12:323-326.. De Castro,J. 1. & R.M,Newson. 1"993. HostresÍst\lllce in cattlt: lickcontrol.. FAO.. PáraSitol. Today 9:. 13e17... 1990: Report of the FAOExpertConsultation on rev;. sion of strategies for the contról of ticks and tick-borne diseases. parassitoJogill(Roma). 32: 3-12.. Francis,J. & D. A. Little. 1964. Resistance of Drougfmaster. cattle lO tickinfestation and babesiosis. AusL Ve!. J,40:. 247-253. Frisch,J. E. 1981. Factors affecting the resistance to ecto. ACKNOWLEDdMENTS To the Officers ófCarora Breed Cattlemen Assotiation (ASOCRICA), Carora,Venezuela, to the personnel of ClAC, and to Dei�y Mendoza and María G. Ramír�z, Veterinary Medicine stu dents, for their technical assistance.. and endoparasites of catde in . tropical areas and the irnplications foc selection,p. 17-32. In IABA (ede). Isolopes ando radiatíoíl in Parasit()!ogy IV. Panel Proceeding Series... Herrera.,l}J.. P,ub. 572, Vienna.. 1960. El mestizoPatdo Suizo Carüreilocbmo. base p�un futuro tipo de ganado. Rev. Veto Ve�¡:zoL 9:.. 343-388... .. Meléndez, R. D.&M. Fórlanp. 19%. Incidence al1dinten sity pfBabesia spp, sporokinetesinengorgeq Boophilus. REFERENCES Arteche, C. P. 1987. Consideraciones prácticas sobre el ernpleoderazas resistentes de vaCunos p� la lucha. microplús froma dairy herd in Venezuela.,p. 148-156.. In Camus, E:,J. A. House & .G. Uilenberg. (¡)ditors),. Vector-BomePathogens: Intern ati0l1al Trade and Tropical Animal Díseases. Ann. New York Acad. .. ScL Vol. 791. New York, USA..

(6) REVISTA DE BIOLOGIA TROPICAL. 696. Núñez, 1. L., M. Muñoz·Cobeñas & H. Molledo. 1982.. Boophilus microplus:. The Common Cattle Tick. Springer-Verlag Editors. Berlin, Gerrnany. 204 p.. Roush, R. T. 1993. Ocurrence, genetics and management of insecticide resistance. Parasitol. Today 9: 174-179. Solomon, K. R. 1983. Acaricide resistance in ticks. Adv.. O'Kelly,1. C. & G. W. Seifert. 1969. Relationships between. Veto Sci. Comp. Med. 27: 273-296.. resistance to Boophilus microplus, nutritio.nal status, and blood composition in Shorthorn x Hereford cattle. Aust. J. Biol. Sci. 22: 1497-1506. Roberts, J. A. 1968. Acquisition by the host of resistance to. Villares, 1. B.. 194 L Climatología Zootechnica. IlI.. Contribucao ao estudo da resistencia e susceptibilidade genetica dos bovinos ao Boophilus microplus. Bol. Ind. Anim. (Sao Paulo) 4: 60-80.. the cattle tick Boophilus microplus (Canestrini). 1.. Parasitol. 54: 657-662.. Roberts, J. A. & J. D. Kerr. 1976. Boophilus microplus: passive transfer of resistance in cattle. J. ParasitoL 62:. 485-489.. Wharton, R. H. & K. R. Norris. 1980. Control of parasitic arthropods. Veto Parasitol. 6: 135-164.. Wikel. S. K. 1996. Host irnrnunity to ticks. Annu. Rev. Entomol. 41: 1-22..

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