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Gonadal and extragonadal sperm reserves in Boran and Boran × Friesian bulls raised on two planes of nutrition in the Highlands of Ethiopia
Theriogenology
1992
37:953-961,
cicxacqANDExTRA[;oNADALs~~~INBoRANANDBoRANxFRIFsIAN I4urRlmoNININHIEClTJSF?AISEDoN~pIANEsOF
A. l'kqd,
OF EIMIOPIA
Y. Dembatga and T. Kassa2
l International I&asto& Centm for Africa (ILCA) P.O.E?ox. 5689,Addis Abeba,?CXhicpia 2 Facultyof veterinary P.O.Box
Medicine, 32,
Lkbz
Addis Ababa University
Zeit,Ethicpia
Receivedfor publication: September 11, 1991 Accepted: December 18, 1991
Gonadalan5lextragoEIdalspexm reservesdeteminedintesticular and epididymaltissues cbtained from &ran (1~10)and Eoran x Friesian (1~12)bulls fed either a high or low plane nutritiondiet for a l-year period.Ihe bulls were 32 months of age at castration.Mean (+SEM)daily body weight gains over a l-year period were 776+34 and 264+34 g/day (RO.001) for bulls on high and low nutrition,and their respectivebody weightsatcastrationwere458+17 and 276+17 kg (pCO.01). Meenbodyweights did not differ between Bran and IWan x Friesianbulls. Mean scroLal n-mammntswere 32.120.6 ard 28.850.6 an for the high and Cin=crmference lowplanesof nutrition (RO.01) and 31.8f0.7and 29.2kO.6canforthe Boran and the &ran x Priesian bulls (RO.05). Paired testes and epididymal weightsaveraged432+22and 313222g (FVO.01)ard 46.322.0and 32.9-2.0g (pCO.001)for bulls on the high and lcrwplanes of nutrition,respectively. E!oranx Friesian bulls had significantlyheavier (RO.05) testes, but epididymalweights did not differ bebreeds. Although daily sperm prcductionper gram was not influencedby eim plane of nutritionor breed, daily spempm&.ztiondiffered betweenhigh (5.3 x 109)and law nutrition(2.9x 10')bulls (p
Keywords:zebu,cm6sbrXd,bul1s,spXm
reserves,nutrition,genotrpe
INIRXWCJX~ Morethan85%ofthecalvesbominthetrapicsaresired~M~ mating, andthe importanceof an iklividualMl in influencing herd fertilityand it's significant contribution to geneticimproven?ent in both naturallyard artificiallybred herds has been highlightedin a recent review (1).Reprociuctivep&entialof ZebubullshasbeenreportedinAfrica Acmowledgments The authors thankMs. HirutMulugeta andMr. Kasshun Zewdie for the technicalassistanceand Mr. Anare Atale for data analysis.
Copyright
Q 1992
Butterworth-Heinemann
954
Theriogenofogy
(5).lbesest&ies have (2, 3), in Australia (4) and in Iatin mica ~icatedal~repraductivepotentidlinBosindicus~inBostaurus breeds ti variations in the repzmluctive p&e&ial Within E3%-irxlia1~ breeds. Ihebullispartidllyresponsibleforthel~fertilityofcows inthe Zebubreed (6).Nutritioninfluencestesticulargmwth,spermproduction capacityandfertility,particularlyinthetropicSwhere seasmalityinthe quantityarbdqualityoffeedisseVere (6,7).JWmhaqh~~inbull reproductivetraitshavebeenreportedinZel=uandQmsbredbLzlsthrough proteinsupplmentation(7- 9), studiesonthe effectsof nutritionon the ~~~ivepotentidLofBosindicusbulls~their~ inAfricaare imdequatetidate. ~eBoranb~isoneofthemzstp~singbeefb~inBasternand southeastern Africa (10).However,data on the reproductivepotentialof mosses with exotic breeds are bullsofmis imdigemls breed&its limited.lhisstudyprovidesinfonnationonyonadalandexl~~gonadalqerm reservesinyoungBoranandEmanxFYiesiancroesbredbulls fedeithera high or low plane of nutritionfora periodof one year.
Station 'Ihestudywasuodertakmby the IICAatthe C&re zeit &search located50 kmsc~w of AddisAbaba. Thestationis situatedat8'44'Nand 39°02qEatanaltitude,185011~matmual rainfallis 8661q of which 84% fallsduring the long rainy season (Juneto SepM&er). Mean m.inhum an3 m&mum temperaare 10.6.0 and 25.6OC,respectively,the overall averagebeing 18.?C. Ten~~ard12Boranx~iesianbulls~usedforthe~.Wi~ genotype,bulls were allcca&d to eithera high or lm plane of nutrition. Theaverageageardbcdyweightofkxll1swere20.2+0.5monthsand225.5+2.5 kg, respectively. All bulls wers providedwith grasshay arxl green alfalfa crop. wills on hi* plane of nutritionreceived an additionalration campcsedofnoug(Cuizotiaabvssinica) mkeandwheatbran.wiLlsweregxmp fedforapericdofoneyear,andtheamuntoffe0dofferedwasadjustedon thebasisofweeklybadyweightstoyieldgrc%&hratesof750and250g/day inthehigh amdlowplaneof nutritiongrcqs,respectively. The bulls were hausedunderanopenshadeandhadf~a~tOwaterarrlminerdLlicks. Dataonbodywei$-~ta&scrotalcircmfermce (SC)werecollectedbefore the bulls were surgicallycastratedat an average age of 32 months. Genitaliawerereimved,arKlthetestesweredissected freeofany&Xanems tissue.~eepidictymiswasseparatedfrosn~~isanddividedintocaFRlt, mrpusardcaudasegmentsbasedongrossanatcany.Testisandepidi~s segment weights were recotied.Approximately20 to 25 g of testicular parenchymlsampleeandepididymal segmmtswerecolleotedunilaterallyfrom the right testis and kept frozenat -15°Cuntilprocess&. Estirmtesof testimlarandepididyml spermreservesweredetemined by the hmcgenization techniquesdescribedin earlierreports (11, 12). A time divisor of 5.11 calculatedfor B indicusbulls (13) was used to calculatedailyspemprortuctionpergram. me effect of plane of nutritionon body weight, SC, testicularard epididymlweights,dailysparmprcductionpergram, dailysparmpmduction,
Theriogenology
amlysis of andepidi~ spmn reserves~analyzedbyleastsquares 0ftheSAspmgram varianceus.~theGemXal LiEmmckls(GrM)plmcedWe (14).~~i~twasusedasacxJvariateinthermdel.Correlationanalysis
Data on body weight, testkular chamkeristics, ard gomdal and @SEX) age extragonadalqerln?XsemesarepzSmted in Table 1. Them oflmllswas 32+0.5marrthsanddidnotdifferbetneen~~ional treatment bulls onthehighplana of nutrition groups~genotypes. At castrations, weresignifkantlyheavier (FWO.001) by182 kg (66%)thanbulls onlowplans of nutrition, buttherewasnodifferencebetmmBoranandBoranxFkiesian breedkiLls.Meandailybody~i~tgainsduring~l-yearstudyperiodwas significantlyhigher (pCO.001)in the high than in the low plane of mtrition (776f34 vs 264234 g/day). The SC mBasurementalso differed significantly(RO.01) betweenthe high and lw plans nutritionbulls and htwe=genotypes (RO.05). Although bulls on high plans of mkrition had 3.3 anlazVerSCthanbullscnlawplaneofnutriti~,theSC:~~i~t ratio was higher in low plans (1.04)than in high plane nutritionbulls (0.70).A hi@ plane of mkrition increasedSC by 12% in both gemtypes. Pairedtestesm&htswere influenc&b0thbyplaneofnutritionand genotypa.Bulls onhighplane of nut?zitionhad 38% heavier (P-zO.01) testes than those on low plans of nutrition,and Bran Mls had a 27% heavier iKO.05) testes than Eman x l?t&sianbulls. Ahigh plans of nutrition Im=reasedpairedtestes~i~tby35and43%inBoranardB0ranx~iesian bulls,respectively.Differencesbetweentherightandlefttestisweight was less than 10% in all gxcups. Paired epididymalweights were also significantly(p
956
Theriogenology
distributionincaprt,corpusardcauddlserpnentsrangedfropn28to21%,10 to 13% and 54 to 62%, respectively, andwerenot infhencedby of nutrition or genotype. Tablel.
eitherplane
Ieastsquaresmeans gram (IXFG), daily spsxmprcduction (IXP), and epididymal reserves (ESR) inBoranardBoranxFriesianbullsaneitheralaw or high plane of nutritiona. Nutrition
plans Bo?can
Traits
0-w
Age WntW E!odyweight
(kg)
32.0f0.9 276.0&15.0 28.82 0.6
SC (a)
sperm
EBranxFYiesian 0-12)
32.3% 0.9 458.0&17.0***
30.4c_ 0.9 358.el8.0
32.15 0.6**
31.8+ 0.7
33.4+
0.9
377.w16.0 29.2+ 0.6*
Testesweight Right testis Left testis Pairedtestes Epididyml
weight
mtiit
(x106)
IEP (xlO9)
216.0+_13.6** 216.3+10.5** 432.4+22.3**
211.8kl4.2 205.6+11.0 417.ti23.3
156.5+13.0** 171.qt10.0* 328.3+21.3*
(g) 17.3+ 1.2 5.0+_ 0.4 10.3+ 0.9 32.5+ 2.0
caput corpus cauda
D6FG
152.2213.6 161.2+10.5 313.4k22.3
7.3t1.5 2.9& 0.2
24.1&1.2*** 7.2+ 0.4*** 15.of 0.9*** 46.3+ 2.0*** 10.2+1.5 5.32 0.2***
21.1+ 6.6+ 13.w 41.e
1.2 0.4 1.0 2.1
20.3k1.2 5.6+_ 0.4 11.3+ 0.9 37.2+ 2.0
8.8k1.6
8.7k1.4
4.Q
3.5+_ 0.2**
0.2
ESR (xlO9) 2.1+ 0.e 4.e 6.9t
caput corpus caL&
rnw
0.3 0.1 0.8 0.9
4.22 1.6+ 7.4% 13.2+
0.3*** 0.1** 0.8** 0.9***
4.3+ 0.3 1.7+ 0.1 6.9+ 0.8 12.9-& 0.9
2.qt_ 0.72 4.42 7.1+
Relative sperm distritution in epididymal segments (%) 30.0 13.0 57.0
caput -VJs cauda
a Between *
** ***
treamts
RO.05. RO.01. Pco.001.
arKi
32.0 12.0 56.0
genotype.
33.0 13.0 54.0
28.0 10.0 62.0
0.3*** 0.1*** 0.7* 0.9**
957
Theriogenology
Importantooefficientsofoorrelation~faYdbetween~wei~t~ SC, between SC ard paired testes weight, between SC arrldaily sperm production,ard bepaired testes weight and daily sperm production (Table2). Table 2. Significant coefficientsof correlationbetween body weight (EWr),scrotalcirunnf~ (SC),pati atf=~ =i*t WV, epididymal~i~t(EwT),dailyspermp~ionpergram(~R;), dailys.pempmduction (iXP),axx3epididymalqem-=(=a inBoran (Wediagonal) andBoranxhiesian (bekwdiagonal) bulls.
ml?
SC
Pm
Esm
ClsP
ESR
EaJT
-
0.84**
0.81**
0.92***
0.91***
0.85***
SC
O-82***
-
0.80**
0.72*
0.79**
0.70*
PIW
0.71**
0.75**
-
0.77**
0.87***
0.75*
?zwr
o-91***
0.86***
0.89***
-
0.91**
0.88***
c6P
0.87***
0.79**
o-88***
0.92**
-
0.96***
ESR
0.78**
0.59*
-
0.66*
0.68*
-
* RO.05. ** RO.01. *** pc0.001. DISCUSSION Differencesingrcwth zatesbetweenkmlls onhighandlawplanes of nutritionresultedin a 66% differencein kcdy weight at castrationwhich wasassociat&witha12% increaseinSC.Bodyweights~thesebullswe.re similarto that reported for 2.5- to 3.5-year-oldE!oeirdicus bulls in Australia(4),where a differenceof 46% inb&yweight between age gmqx resultedin a 19% differenceinSC.Inbothgemtypes,theSCwassmaller thanthe 34 anreportedforn&ureEmajiandSokotokxlls inNigeria (3)and bulls in Florida (15). for young W A high plane of nutritionimreas& testesweight confirmiq that the spermproducir~~, testicularparenchymaltissue is labile to nutritional treatrnents(6).~insupplementationtOBosindicusbullscfuringthedry season had positivelyinfluencedbcdy weight,testicularsize and sperm SC arkitestesweight (4, 16) pxxduction(7).The stzmq asscciationbetween isalsoccnfirmed inthepre.sentstucty,wherea12%difference inthe SC between bulls on high and 1~ plane diets was associatedwith a 38% differencein testes weight ard a 9% differerceinscbetweenEoranard E~1ranxFriesianbreedbullswasassociatedwitha27%differenceintestes weight.
958
Theriogenology
Pairedtestesk~i~~of418and328gintheBoranardBoranxR-iesian bulls found in this study wsma heavierthan the 224 g report& for Nelore bulls inBrazil (5)amdlighterthanthe 354 gmqortad for other Zebmbulls (2).AlthoughBoran bulls had 89qheavier testes than Boran x kiesian ~ls,thesewei~~~li~~thanthe67OgreportedformatureBrahman cmss bulls (4) and canparableto the 412 g reportedfor mature Sokoto Gudali~ls(3).BoranxFriesian~lsdLsohadccmparable~~i~~ toZebuC.KCssbulls of the sams age in trcpicalAustralia(4). lhesignificanteffectofnutritiononepididymlw+aightfaundinmr study is similarto that of an earlierfinding(17),in which Herefordand An3usbullsfeda~~energydiethadheavierepididymdL~i~~thanthose fedamsdiumsnergydiet. Ihcmtrast, hawwer, vaulterand Bailey (18), workiqontbesamabrseds,didmtfindanysignificanteffectofdi&ary ensqy on spididymalweights.!lhedisparity betweentheseresultscouldbs due tovariatiohsin age of animals,guantityard gualityof feed offered, andthedurationoffeeding.EpidictymdLweights i.nbothBoranardBoranX FYissianbullsweresimilartothcSeofAngonaTd bartosebulls inAfrica (2)and zebu cress bulls in Australia(4). The absenceof nutritionaleffectsand genotypsdifferencesin daily sperm productionper gram,cmfirms that in a given species daily sperm praluctionpar gram is nummally affectedby envizcmkahtalfactors (19). prctein supplemmtation has also besn found not to affect daily spars prcdudionpergram inotherE?csirdicusbulls(7).Estimatesofdaily+enn prdluctionpergraminbothgMotypes~slilpltlyl~thanthevdlues reportedfor other Bos tiicus breeds (2, 7) but ware aqmrable to the valuesgiven for Zebu cresses(4)arYdEC6 taurusbezflX.llls (20).Moreover, thev~witkintheranseofMluesreportedforbothBosindicusandBos taGus bulls (2, 5, 20, 21). Oaily sperm prcduction,which is depemdsntprimarilyon the awunt of spermproducing,testicularparenchymdltissue,ishi~ycorrelatedwith testesweight(4,20). The significant effect of nutrition on testesweight and hence on daily sperm prcductionconfirm earlier findings (22, 23). Estimatesofdailyspermpmdudioninthe~genotypeswerelawerthanthe sstin-ates for EC6 tam-usbreeds (11,20),theyr canparableIXYestimates forotherE!osindimstulls(2,3),andwerehighertbanthsvalusforNelore bulls (5).Eman bulls had similarestimtss of daily spem prcductionto bartcseand Africmder bulls (2)‘EQXhmanbulls (7) andzetalcrossbul1s (4),whileBoranxhiesianbullshadsimilardailyspermprdductionvalues to Sokoto Gudali and Angon bulls (2, 3). The high positive correlation bstmaentestesweightanddailyspermprcductioninbothbreeds showsthe closerslationshipbetweenthetw0traits.As a result,a 38% differencein testeswei~~betweenbvillsonhi~andlawplanedietswas associatedwith 83% diffsxencein daily sperm productionand a 27% diffemnce intestes weight between Em--anand Boranx FriesianbUlswas associatk3d with 31% differencesin daily spermproduction. The significanteffsct of plans of nutrition on epididyml spenn reserveslends Supportto earlierfindings(17, 18) in which epididymal spermreserveswerehi~~in~lsfedamediumenergydietthanahiZPl energy diet. Estimatesofepididymalqem reservesinthetwogemtypes wsre muchlawsr than the values reportedfor Bos taurus dairy and beef b& (11,20), forotherF?osiI?dicuSbreeds i.ntropicdlAfrica (2,3), and forBrahmahcmss bullsintrapicalAustrdLia(7).However,epididymdlsperm reserve.5ih Boran bulls cxmpar& well with the values report& for
Theriogenology
959
Africanderand other Zebu bulls (2), while the estimates for Hcran x FriesiankillscanparedwellwiththevdluesreportedforBaladyardcsther zebu bills (24, 25). Fewer epididymalspem reservesthanfamdinthe presMtstudyhavedLsobeenreportedforZelxlcrossbyllsin~icdl Australia(4). The rarqe of 54 to 62% in relativespezm distributionin the cauda epididymis~inbothgenotypeSwassimilartOthemeanvdLueof52%reported forHrahzen~~1~(4);~~,sli~~y~~~estimates~ingfrcan 57to72%havel~enreportedforotherZeku~lsinAfrica (2,3).lhe relativelyhi~percentageofspermcellsin~ca~thaninthecaplt ticoxpusepididymal sqmentsalsoamfimsthatit isthemajorsiteof spem storage (2 - 4). SCandpairedtestesweigli~and Thehigh,pcsitiveccrrelationsbetween ccnfim earlier betweenSCamddailyspennpruluctioninbothgenotypes results.~~a~~betweentestes~i~tanddailyspermp~~have also bean fcmd to range frm 0.70 to 0.85. These high, positive relationshipsbetween SC ard testes weight and daily spenn production imlicatethatSC measurtsnentswuldbeus&toestin&etesticularweight andspermproducing~cityofthetestis.Moreover,~ inSC v selection for larger testis size and/or inprovednutrition and managementcculd imprcvetestis size and the sperm-p-ion capacityof bulls. Insunrmary,theresultsofthisstudyconfirmearlierreportsthatthere aregenotypediffeEnces a.rdnutritionalinfluencez onbcdyweight, testis size, andweightaswellas ongonadal arxlepididymal sperm reserves.lbe nutritionalstatusof bulls and genotypedifferences havetobetakeninto account, therefore, in planning either natural mating or artificial insemimtionprogram.Fu.rtherstudiesusinglaqermmkers of arlimlls hcwever,arewarrantedtodetenninethelong-temeffectsofvaryingplanes ofnutritiononthereproductivetraitsandfertilityofdifferentgenoQpes of bulls. The establishmentand incorporation of reprcductivetraits in selectionproceduresofZelmandcmssbmdb.llscouldccntriJmtenctonly to inprovementsin reprcductivecapacityof bulls but also to cowherd reprcductionarsdfertilityintrcpicalregions.
1. Galina, C.S. and Arthur, G.H. F&view of cattle reprcductionin the tropics.Part 6. Theme. Anim. Breed.Abstr.=:403-412 (1991). 2. Iglxrali, G. and-, A.M. Gmadal and extragonadal sperm rese.rves of irdigenouscentral Africanbulls. J. Reprcd.Fertil.~:107-109 (1971). 3. Salau-Dauctu, C. and Shoyinka,V. Scmtalcircumf~, daily spexm prcductionand epididyml spezmatozoaof the irrdigenous Hunaji and SokotoGudalibulls in Nigeria.Hr. Vet. J. =:467-470 (1983). 4. Wildeus, S. and Krkwistle,K.W. Fcst@ertal &larqes in gonadal and extragonadalspenn reservesinEcsindicusstrainbulls.'Ihericgemlogy =:655-668 (1982). 5. cardoso,F.M. and Gcclinho, H.P. Daily spem pruluctionof Zeku (& indicus) estimated by guantitative histology of the testis. lheriogenolcgy =:841-847 (1985).
Theriogenology
6.
Entwistle,K.W. Factors influencingreproductionin beef cattle in Australia.Aust.~tResear& CouncilReviei?No. a:l-30 (1983).
7.
Ndama, P.H., Entwistle,K.W. and Lindsay,J.A. Effect of pmtected prcteinsup@smantonscmetesticulartmitsin Brahmancress bills. l'hericgemlcgy =:639-650 (1983).
8.
Rekwot,P.I.,Oyedipe, E.O.,Akarejola,O.O.,Kusi-Diaka,J. a~~lUmh, J.E. ?he effectof protein intabontheonsetofpxberty in Bunajiand Friesianx Bunajicrcssbmd bulls.lheriogenolcgy =:427-434 (1987).
9.
Fekwot, P.I., Oyedipe,E.O., Akerejola,0.0. and Kumi-Diaka,J. Ihe effectofpmteinintakeonlxdywaight, -C--andpr0ductionofl%majibullsandtheirFriesiancmssesinNigeria.?mim. Reprcd. Sci. x:1-9 (1988).
10.
Alberm, M.arx? Hail~iam,S.'IheindigenauscattleofMhiopia.Part II. Wld. Anim. Rev. &:27-42 (1982).
J.O. andAmnn, R.P.Reprcductivecapacifyofdairybulls. II. 11. Ahquist, Gonadalandextragonadalspem reservesasdetemunedbydirectccunts amddepletiontrials;dimansionsaxlweightofgenitalia. J. Dairy Sci. u:1668-1678 (1961). of daily 12. Amann, R.P. and Ii&&se, J.T. The male r&bit. Determination spennproductionbymeans of testicularhcmcgmization.J. Anim. Sci. =:369-374 (1969). 13. Salin, B. and Entwistle,K.W. bxation of the seminiferousepithelial cycle in hybrid Bee indicusx Bos tawus Bulls. J. Reprod. Fertil. &:729-734 (1982). AnalysisSystem.Guy, NC, 1987. 14. SASUserlsManual.Statistical 15. Fields,M.J., Hentges,J.F., Kenneth, W. and Comelisse, K.W. Aspects of sexual develo$msntof Brahmn versus Angus bulls in Florida, Thericgemlogy=:17-31 (1982). in m indicus cattle in Northern 16. Entwistle, K.W. Reprccluction Australia.Prcc.Aust. See. Anim. Prud.s:60-61 (1980). G.H.,Carruthers, T.D.,Amann,R.P. a~xdKozub, G.C. Testicular 17. Cailter, develop&nt,dailyspennprodudionandepididymal spermresemesin15me-old ~mgus and HerefordBulls: effectsof bull strainplus dietary energy.J. Anim. Sci. a:254-260 (1987). spermreservesin12-mnth18. Cculter,G.H. a&Bailey, D.R.C.Epididynbal old Angus and Hereford bulls: effects of bull strain plus dietary energy.Anim. Reprcd.Sci. s:169-175 (1988). 19. m, M-‘ Hccheraeude Reviers, M.T. and O&avant, R. Spermatogerwsis. In: Jchnson,A.D., Ganes, W.R. and VanDemark,N.L. (e&s.),meTestis. Vol. I. AcademicPress,NewYork, 1970,pp.339-432. J.O. Reprcductive capacityof beef bulls: 20. Weisgold,A.D. and -St, dailyspennatczoalproduction,spermatczoalresemes,anddimmsions ard weightsof reproductive organs.J. Anim. Sci. M:351-358 (1979).
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961
21. MacMillan, K.L., Newhook, C. atxlWatson, J.D. Testiailarandepidi~ sperm rnmbx-s in young F'riesianbulls. N.Z. J. Agri. F&s. s:255-259 (1972). 22. V-k, N-L. tiMauger, R.E. Effectofeneqy intakeonreproductive perfoxmnce of dairy bulls. I. Growth of reproductive ozqam ad pberty. J. Eairy. Sci. =:798-802 (1964). 23. caulter, G.H. Testiadardevelopmt: it's ma+pmmtandsignificance inyomqbeefbulls. PJTUC.8*'Ibch.Conf. AI andRqmd. pi. l-6 (1981). 24. Osman, A.M. andEl-Azab, E.A. Stuliesonqonadal andextmgonadal reserves in BdLadyhiLls. Anim. Breed. At&r. 43:457 (1974). 25. El-&&, E.A. 'Ibstidarandqidi~ Sudan. Anim. Breed. Ah&r. a:349
spzrm
sperm reservesinzebubillsin (1976).
1992
37:953-961,
cicxacqANDExTRA[;oNADALs~~~INBoRANANDBoRANxFRIFsIAN I4urRlmoNININHIEClTJSF?AISEDoN~pIANEsOF
A. l'kqd,
OF EIMIOPIA
Y. Dembatga and T. Kassa2
l International I&asto& Centm for Africa (ILCA) P.O.E?ox. 5689,Addis Abeba,?CXhicpia 2 Facultyof veterinary P.O.Box
Medicine, 32,
Lkbz
Addis Ababa University
Zeit,Ethicpia
Receivedfor publication: September 11, 1991 Accepted: December 18, 1991
Gonadalan5lextragoEIdalspexm reservesdeteminedintesticular and epididymaltissues cbtained from &ran (1~10)and Eoran x Friesian (1~12)bulls fed either a high or low plane nutritiondiet for a l-year period.Ihe bulls were 32 months of age at castration.Mean (+SEM)daily body weight gains over a l-year period were 776+34 and 264+34 g/day (RO.001) for bulls on high and low nutrition,and their respectivebody weightsatcastrationwere458+17 and 276+17 kg (pCO.01). Meenbodyweights did not differ between Bran and IWan x Friesianbulls. Mean scroLal n-mammntswere 32.120.6 ard 28.850.6 an for the high and Cin=crmference lowplanesof nutrition (RO.01) and 31.8f0.7and 29.2kO.6canforthe Boran and the &ran x Priesian bulls (RO.05). Paired testes and epididymal weightsaveraged432+22and 313222g (FVO.01)ard 46.322.0and 32.9-2.0g (pCO.001)for bulls on the high and lcrwplanes of nutrition,respectively. E!oranx Friesian bulls had significantlyheavier (RO.05) testes, but epididymalweights did not differ bebreeds. Although daily sperm prcductionper gram was not influencedby eim plane of nutritionor breed, daily spempm&.ztiondiffered betweenhigh (5.3 x 109)and law nutrition(2.9x 10')bulls (p
Keywords:zebu,cm6sbrXd,bul1s,spXm
reserves,nutrition,genotrpe
INIRXWCJX~ Morethan85%ofthecalvesbominthetrapicsaresired~M~ mating, andthe importanceof an iklividualMl in influencing herd fertilityand it's significant contribution to geneticimproven?ent in both naturallyard artificiallybred herds has been highlightedin a recent review (1).Reprociuctivep&entialof ZebubullshasbeenreportedinAfrica Acmowledgments The authors thankMs. HirutMulugeta andMr. Kasshun Zewdie for the technicalassistanceand Mr. Anare Atale for data analysis.
Copyright
Q 1992
Butterworth-Heinemann
954
Theriogenofogy
(5).lbesest&ies have (2, 3), in Australia (4) and in Iatin mica ~icatedal~repraductivepotentidlinBosindicus~inBostaurus breeds ti variations in the repzmluctive p&e&ial Within E3%-irxlia1~ breeds. Ihebullispartidllyresponsibleforthel~fertilityofcows inthe Zebubreed (6).Nutritioninfluencestesticulargmwth,spermproduction capacityandfertility,particularlyinthetropicSwhere seasmalityinthe quantityarbdqualityoffeedisseVere (6,7).JWmhaqh~~inbull reproductivetraitshavebeenreportedinZel=uandQmsbredbLzlsthrough proteinsupplmentation(7- 9), studiesonthe effectsof nutritionon the ~~~ivepotentidLofBosindicusbulls~their~ inAfricaare imdequatetidate. ~eBoranb~isoneofthemzstp~singbeefb~inBasternand southeastern Africa (10).However,data on the reproductivepotentialof mosses with exotic breeds are bullsofmis imdigemls breed&its limited.lhisstudyprovidesinfonnationonyonadalandexl~~gonadalqerm reservesinyoungBoranandEmanxFYiesiancroesbredbulls fedeithera high or low plane of nutritionfora periodof one year.
Station 'Ihestudywasuodertakmby the IICAatthe C&re zeit &search located50 kmsc~w of AddisAbaba. Thestationis situatedat8'44'Nand 39°02qEatanaltitude,185011~matmual rainfallis 8661q of which 84% fallsduring the long rainy season (Juneto SepM&er). Mean m.inhum an3 m&mum temperaare 10.6.0 and 25.6OC,respectively,the overall averagebeing 18.?C. Ten~~ard12Boranx~iesianbulls~usedforthe~.Wi~ genotype,bulls were allcca&d to eithera high or lm plane of nutrition. Theaverageageardbcdyweightofkxll1swere20.2+0.5monthsand225.5+2.5 kg, respectively. All bulls wers providedwith grasshay arxl green alfalfa crop. wills on hi* plane of nutritionreceived an additionalration campcsedofnoug(Cuizotiaabvssinica) mkeandwheatbran.wiLlsweregxmp fedforapericdofoneyear,andtheamuntoffe0dofferedwasadjustedon thebasisofweeklybadyweightstoyieldgrc%&hratesof750and250g/day inthehigh amdlowplaneof nutritiongrcqs,respectively. The bulls were hausedunderanopenshadeandhadf~a~tOwaterarrlminerdLlicks. Dataonbodywei$-~ta&scrotalcircmfermce (SC)werecollectedbefore the bulls were surgicallycastratedat an average age of 32 months. Genitaliawerereimved,arKlthetestesweredissected freeofany&Xanems tissue.~eepidictymiswasseparatedfrosn~~isanddividedintocaFRlt, mrpusardcaudasegmentsbasedongrossanatcany.Testisandepidi~s segment weights were recotied.Approximately20 to 25 g of testicular parenchymlsampleeandepididymal segmmtswerecolleotedunilaterallyfrom the right testis and kept frozenat -15°Cuntilprocess&. Estirmtesof testimlarandepididyml spermreservesweredetemined by the hmcgenization techniquesdescribedin earlierreports (11, 12). A time divisor of 5.11 calculatedfor B indicusbulls (13) was used to calculatedailyspemprortuctionpergram. me effect of plane of nutritionon body weight, SC, testicularard epididymlweights,dailysparmprcductionpergram, dailysparmpmduction,
Theriogenology
amlysis of andepidi~ spmn reserves~analyzedbyleastsquares 0ftheSAspmgram varianceus.~theGemXal LiEmmckls(GrM)plmcedWe (14).~~i~twasusedasacxJvariateinthermdel.Correlationanalysis
Data on body weight, testkular chamkeristics, ard gomdal and @SEX) age extragonadalqerln?XsemesarepzSmted in Table 1. Them oflmllswas 32+0.5marrthsanddidnotdifferbetneen~~ional treatment bulls onthehighplana of nutrition groups~genotypes. At castrations, weresignifkantlyheavier (FWO.001) by182 kg (66%)thanbulls onlowplans of nutrition, buttherewasnodifferencebetmmBoranandBoranxFkiesian breedkiLls.Meandailybody~i~tgainsduring~l-yearstudyperiodwas significantlyhigher (pCO.001)in the high than in the low plane of mtrition (776f34 vs 264234 g/day). The SC mBasurementalso differed significantly(RO.01) betweenthe high and lw plans nutritionbulls and htwe=genotypes (RO.05). Although bulls on high plans of mkrition had 3.3 anlazVerSCthanbullscnlawplaneofnutriti~,theSC:~~i~t ratio was higher in low plans (1.04)than in high plane nutritionbulls (0.70).A hi@ plane of mkrition increasedSC by 12% in both gemtypes. Pairedtestesm&htswere influenc&b0thbyplaneofnutritionand genotypa.Bulls onhighplane of nut?zitionhad 38% heavier (P-zO.01) testes than those on low plans of nutrition,and Bran Mls had a 27% heavier iKO.05) testes than Eman x l?t&sianbulls. Ahigh plans of nutrition Im=reasedpairedtestes~i~tby35and43%inBoranardB0ranx~iesian bulls,respectively.Differencesbetweentherightandlefttestisweight was less than 10% in all gxcups. Paired epididymalweights were also significantly(p
956
Theriogenology
distributionincaprt,corpusardcauddlserpnentsrangedfropn28to21%,10 to 13% and 54 to 62%, respectively, andwerenot infhencedby of nutrition or genotype. Tablel.
eitherplane
Ieastsquaresmeans gram (IXFG), daily spsxmprcduction (IXP), and epididymal reserves (ESR) inBoranardBoranxFriesianbullsaneitheralaw or high plane of nutritiona. Nutrition
plans Bo?can
Traits
0-w
Age WntW E!odyweight
(kg)
32.0f0.9 276.0&15.0 28.82 0.6
SC (a)
sperm
EBranxFYiesian 0-12)
32.3% 0.9 458.0&17.0***
30.4c_ 0.9 358.el8.0
32.15 0.6**
31.8+ 0.7
33.4+
0.9
377.w16.0 29.2+ 0.6*
Testesweight Right testis Left testis Pairedtestes Epididyml
weight
mtiit
(x106)
IEP (xlO9)
216.0+_13.6** 216.3+10.5** 432.4+22.3**
211.8kl4.2 205.6+11.0 417.ti23.3
156.5+13.0** 171.qt10.0* 328.3+21.3*
(g) 17.3+ 1.2 5.0+_ 0.4 10.3+ 0.9 32.5+ 2.0
caput corpus cauda
D6FG
152.2213.6 161.2+10.5 313.4k22.3
7.3t1.5 2.9& 0.2
24.1&1.2*** 7.2+ 0.4*** 15.of 0.9*** 46.3+ 2.0*** 10.2+1.5 5.32 0.2***
21.1+ 6.6+ 13.w 41.e
1.2 0.4 1.0 2.1
20.3k1.2 5.6+_ 0.4 11.3+ 0.9 37.2+ 2.0
8.8k1.6
8.7k1.4
4.Q
3.5+_ 0.2**
0.2
ESR (xlO9) 2.1+ 0.e 4.e 6.9t
caput corpus caL&
rnw
0.3 0.1 0.8 0.9
4.22 1.6+ 7.4% 13.2+
0.3*** 0.1** 0.8** 0.9***
4.3+ 0.3 1.7+ 0.1 6.9+ 0.8 12.9-& 0.9
2.qt_ 0.72 4.42 7.1+
Relative sperm distritution in epididymal segments (%) 30.0 13.0 57.0
caput -VJs cauda
a Between *
** ***
treamts
RO.05. RO.01. Pco.001.
arKi
32.0 12.0 56.0
genotype.
33.0 13.0 54.0
28.0 10.0 62.0
0.3*** 0.1*** 0.7* 0.9**
957
Theriogenology
Importantooefficientsofoorrelation~faYdbetween~wei~t~ SC, between SC ard paired testes weight, between SC arrldaily sperm production,ard bepaired testes weight and daily sperm production (Table2). Table 2. Significant coefficientsof correlationbetween body weight (EWr),scrotalcirunnf~ (SC),pati atf=~ =i*t WV, epididymal~i~t(EwT),dailyspermp~ionpergram(~R;), dailys.pempmduction (iXP),axx3epididymalqem-=(=a inBoran (Wediagonal) andBoranxhiesian (bekwdiagonal) bulls.
ml?
SC
Pm
Esm
ClsP
ESR
EaJT
-
0.84**
0.81**
0.92***
0.91***
0.85***
SC
O-82***
-
0.80**
0.72*
0.79**
0.70*
PIW
0.71**
0.75**
-
0.77**
0.87***
0.75*
?zwr
o-91***
0.86***
0.89***
-
0.91**
0.88***
c6P
0.87***
0.79**
o-88***
0.92**
-
0.96***
ESR
0.78**
0.59*
-
0.66*
0.68*
-
* RO.05. ** RO.01. *** pc0.001. DISCUSSION Differencesingrcwth zatesbetweenkmlls onhighandlawplanes of nutritionresultedin a 66% differencein kcdy weight at castrationwhich wasassociat&witha12% increaseinSC.Bodyweights~thesebullswe.re similarto that reported for 2.5- to 3.5-year-oldE!oeirdicus bulls in Australia(4),where a differenceof 46% inb&yweight between age gmqx resultedin a 19% differenceinSC.Inbothgemtypes,theSCwassmaller thanthe 34 anreportedforn&ureEmajiandSokotokxlls inNigeria (3)and bulls in Florida (15). for young W A high plane of nutritionimreas& testesweight confirmiq that the spermproducir~~, testicularparenchymaltissue is labile to nutritional treatrnents(6).~insupplementationtOBosindicusbullscfuringthedry season had positivelyinfluencedbcdy weight,testicularsize and sperm SC arkitestesweight (4, 16) pxxduction(7).The stzmq asscciationbetween isalsoccnfirmed inthepre.sentstucty,wherea12%difference inthe SC between bulls on high and 1~ plane diets was associatedwith a 38% differencein testes weight ard a 9% differerceinscbetweenEoranard E~1ranxFriesianbreedbullswasassociatedwitha27%differenceintestes weight.
958
Theriogenology
Pairedtestesk~i~~of418and328gintheBoranardBoranxR-iesian bulls found in this study wsma heavierthan the 224 g report& for Nelore bulls inBrazil (5)amdlighterthanthe 354 gmqortad for other Zebmbulls (2).AlthoughBoran bulls had 89qheavier testes than Boran x kiesian ~ls,thesewei~~~li~~thanthe67OgreportedformatureBrahman cmss bulls (4) and canparableto the 412 g reportedfor mature Sokoto Gudali~ls(3).BoranxFriesian~lsdLsohadccmparable~~i~~ toZebuC.KCssbulls of the sams age in trcpicalAustralia(4). lhesignificanteffectofnutritiononepididymlw+aightfaundinmr study is similarto that of an earlierfinding(17),in which Herefordand An3usbullsfeda~~energydiethadheavierepididymdL~i~~thanthose fedamsdiumsnergydiet. Ihcmtrast, hawwer, vaulterand Bailey (18), workiqontbesamabrseds,didmtfindanysignificanteffectofdi&ary ensqy on spididymalweights.!lhedisparity betweentheseresultscouldbs due tovariatiohsin age of animals,guantityard gualityof feed offered, andthedurationoffeeding.EpidictymdLweights i.nbothBoranardBoranX FYissianbullsweresimilartothcSeofAngonaTd bartosebulls inAfrica (2)and zebu cress bulls in Australia(4). The absenceof nutritionaleffectsand genotypsdifferencesin daily sperm productionper gram,cmfirms that in a given species daily sperm praluctionpar gram is nummally affectedby envizcmkahtalfactors (19). prctein supplemmtation has also besn found not to affect daily spars prcdudionpergram inotherE?csirdicusbulls(7).Estimatesofdaily+enn prdluctionpergraminbothgMotypes~slilpltlyl~thanthevdlues reportedfor other Bos tiicus breeds (2, 7) but ware aqmrable to the valuesgiven for Zebu cresses(4)arYdEC6 taurusbezflX.llls (20).Moreover, thev~witkintheranseofMluesreportedforbothBosindicusandBos taGus bulls (2, 5, 20, 21). Oaily sperm prcduction,which is depemdsntprimarilyon the awunt of spermproducing,testicularparenchymdltissue,ishi~ycorrelatedwith testesweight(4,20). The significant effect of nutrition on testesweight and hence on daily sperm prcductionconfirm earlier findings (22, 23). Estimatesofdailyspermpmdudioninthe~genotypeswerelawerthanthe sstin-ates for EC6 tam-usbreeds (11,20),theyr canparableIXYestimates forotherE!osindimstulls(2,3),andwerehighertbanthsvalusforNelore bulls (5).Eman bulls had similarestimtss of daily spem prcductionto bartcseand Africmder bulls (2)‘EQXhmanbulls (7) andzetalcrossbul1s (4),whileBoranxhiesianbullshadsimilardailyspermprdductionvalues to Sokoto Gudali and Angon bulls (2, 3). The high positive correlation bstmaentestesweightanddailyspermprcductioninbothbreeds showsthe closerslationshipbetweenthetw0traits.As a result,a 38% differencein testeswei~~betweenbvillsonhi~andlawplanedietswas associatedwith 83% diffsxencein daily sperm productionand a 27% diffemnce intestes weight between Em--anand Boranx FriesianbUlswas associatk3d with 31% differencesin daily spermproduction. The significanteffsct of plans of nutrition on epididyml spenn reserveslends Supportto earlierfindings(17, 18) in which epididymal spermreserveswerehi~~in~lsfedamediumenergydietthanahiZPl energy diet. Estimatesofepididymalqem reservesinthetwogemtypes wsre muchlawsr than the values reportedfor Bos taurus dairy and beef b& (11,20), forotherF?osiI?dicuSbreeds i.ntropicdlAfrica (2,3), and forBrahmahcmss bullsintrapicalAustrdLia(7).However,epididymdlsperm reserve.5ih Boran bulls cxmpar& well with the values report& for
Theriogenology
959
Africanderand other Zebu bulls (2), while the estimates for Hcran x FriesiankillscanparedwellwiththevdluesreportedforBaladyardcsther zebu bills (24, 25). Fewer epididymalspem reservesthanfamdinthe presMtstudyhavedLsobeenreportedforZelxlcrossbyllsin~icdl Australia(4). The rarqe of 54 to 62% in relativespezm distributionin the cauda epididymis~inbothgenotypeSwassimilartOthemeanvdLueof52%reported forHrahzen~~1~(4);~~,sli~~y~~~estimates~ingfrcan 57to72%havel~enreportedforotherZeku~lsinAfrica (2,3).lhe relativelyhi~percentageofspermcellsin~ca~thaninthecaplt ticoxpusepididymal sqmentsalsoamfimsthatit isthemajorsiteof spem storage (2 - 4). SCandpairedtestesweigli~and Thehigh,pcsitiveccrrelationsbetween ccnfim earlier betweenSCamddailyspennpruluctioninbothgenotypes results.~~a~~betweentestes~i~tanddailyspermp~~have also bean fcmd to range frm 0.70 to 0.85. These high, positive relationshipsbetween SC ard testes weight and daily spenn production imlicatethatSC measurtsnentswuldbeus&toestin&etesticularweight andspermproducing~cityofthetestis.Moreover,~ inSC v selection for larger testis size and/or inprovednutrition and managementcculd imprcvetestis size and the sperm-p-ion capacityof bulls. Insunrmary,theresultsofthisstudyconfirmearlierreportsthatthere aregenotypediffeEnces a.rdnutritionalinfluencez onbcdyweight, testis size, andweightaswellas ongonadal arxlepididymal sperm reserves.lbe nutritionalstatusof bulls and genotypedifferences havetobetakeninto account, therefore, in planning either natural mating or artificial insemimtionprogram.Fu.rtherstudiesusinglaqermmkers of arlimlls hcwever,arewarrantedtodetenninethelong-temeffectsofvaryingplanes ofnutritiononthereproductivetraitsandfertilityofdifferentgenoQpes of bulls. The establishmentand incorporation of reprcductivetraits in selectionproceduresofZelmandcmssbmdb.llscouldccntriJmtenctonly to inprovementsin reprcductivecapacityof bulls but also to cowherd reprcductionarsdfertilityintrcpicalregions.
1. Galina, C.S. and Arthur, G.H. F&view of cattle reprcductionin the tropics.Part 6. Theme. Anim. Breed.Abstr.=:403-412 (1991). 2. Iglxrali, G. and-, A.M. Gmadal and extragonadal sperm rese.rves of irdigenouscentral Africanbulls. J. Reprcd.Fertil.~:107-109 (1971). 3. Salau-Dauctu, C. and Shoyinka,V. Scmtalcircumf~, daily spexm prcductionand epididyml spezmatozoaof the irrdigenous Hunaji and SokotoGudalibulls in Nigeria.Hr. Vet. J. =:467-470 (1983). 4. Wildeus, S. and Krkwistle,K.W. Fcst@ertal &larqes in gonadal and extragonadalspenn reservesinEcsindicusstrainbulls.'Ihericgemlogy =:655-668 (1982). 5. cardoso,F.M. and Gcclinho, H.P. Daily spem pruluctionof Zeku (& indicus) estimated by guantitative histology of the testis. lheriogenolcgy =:841-847 (1985).
Theriogenology
6.
Entwistle,K.W. Factors influencingreproductionin beef cattle in Australia.Aust.~tResear& CouncilReviei?No. a:l-30 (1983).
7.
Ndama, P.H., Entwistle,K.W. and Lindsay,J.A. Effect of pmtected prcteinsup@smantonscmetesticulartmitsin Brahmancress bills. l'hericgemlcgy =:639-650 (1983).
8.
Rekwot,P.I.,Oyedipe, E.O.,Akarejola,O.O.,Kusi-Diaka,J. a~~lUmh, J.E. ?he effectof protein intabontheonsetofpxberty in Bunajiand Friesianx Bunajicrcssbmd bulls.lheriogenolcgy =:427-434 (1987).
9.
Fekwot, P.I., Oyedipe,E.O., Akerejola,0.0. and Kumi-Diaka,J. Ihe effectofpmteinintakeonlxdywaight, -C--andpr0ductionofl%majibullsandtheirFriesiancmssesinNigeria.?mim. Reprcd. Sci. x:1-9 (1988).
10.
Alberm, M.arx? Hail~iam,S.'IheindigenauscattleofMhiopia.Part II. Wld. Anim. Rev. &:27-42 (1982).
J.O. andAmnn, R.P.Reprcductivecapacifyofdairybulls. II. 11. Ahquist, Gonadalandextragonadalspem reservesasdetemunedbydirectccunts amddepletiontrials;dimansionsaxlweightofgenitalia. J. Dairy Sci. u:1668-1678 (1961). of daily 12. Amann, R.P. and Ii&&se, J.T. The male r&bit. Determination spennproductionbymeans of testicularhcmcgmization.J. Anim. Sci. =:369-374 (1969). 13. Salin, B. and Entwistle,K.W. bxation of the seminiferousepithelial cycle in hybrid Bee indicusx Bos tawus Bulls. J. Reprod. Fertil. &:729-734 (1982). AnalysisSystem.Guy, NC, 1987. 14. SASUserlsManual.Statistical 15. Fields,M.J., Hentges,J.F., Kenneth, W. and Comelisse, K.W. Aspects of sexual develo$msntof Brahmn versus Angus bulls in Florida, Thericgemlogy=:17-31 (1982). in m indicus cattle in Northern 16. Entwistle, K.W. Reprccluction Australia.Prcc.Aust. See. Anim. Prud.s:60-61 (1980). G.H.,Carruthers, T.D.,Amann,R.P. a~xdKozub, G.C. Testicular 17. Cailter, develop&nt,dailyspennprodudionandepididymal spermresemesin15me-old ~mgus and HerefordBulls: effectsof bull strainplus dietary energy.J. Anim. Sci. a:254-260 (1987). spermreservesin12-mnth18. Cculter,G.H. a&Bailey, D.R.C.Epididynbal old Angus and Hereford bulls: effects of bull strain plus dietary energy.Anim. Reprcd.Sci. s:169-175 (1988). 19. m, M-‘ Hccheraeude Reviers, M.T. and O&avant, R. Spermatogerwsis. In: Jchnson,A.D., Ganes, W.R. and VanDemark,N.L. (e&s.),meTestis. Vol. I. AcademicPress,NewYork, 1970,pp.339-432. J.O. Reprcductive capacityof beef bulls: 20. Weisgold,A.D. and -St, dailyspennatczoalproduction,spermatczoalresemes,anddimmsions ard weightsof reproductive organs.J. Anim. Sci. M:351-358 (1979).
Theriogenology
961
21. MacMillan, K.L., Newhook, C. atxlWatson, J.D. Testiailarandepidi~ sperm rnmbx-s in young F'riesianbulls. N.Z. J. Agri. F&s. s:255-259 (1972). 22. V-k, N-L. tiMauger, R.E. Effectofeneqy intakeonreproductive perfoxmnce of dairy bulls. I. Growth of reproductive ozqam ad pberty. J. Eairy. Sci. =:798-802 (1964). 23. caulter, G.H. Testiadardevelopmt: it's ma+pmmtandsignificance inyomqbeefbulls. PJTUC.8*'Ibch.Conf. AI andRqmd. pi. l-6 (1981). 24. Osman, A.M. andEl-Azab, E.A. Stuliesonqonadal andextmgonadal reserves in BdLadyhiLls. Anim. Breed. At&r. 43:457 (1974). 25. El-&&, E.A. 'Ibstidarandqidi~ Sudan. Anim. Breed. Ah&r. a:349
spzrm
sperm reservesinzebubillsin (1976).