albinele rusesti si varroa

1. INTRODUCTION

In Asia, Varroa destructorAnderson andTruman, 2000 is an innocuous external par-asitic mite of Apis cerana, the Asian hivebee. However, V. destructorhas made a host

shift to Apis mellifera, the western honeybee that is employed world-wide for polli-nating crops and producing honey (Bootet al., 1997; Rath, 1999). The parasite spreadrapidly and now infests most the world’sA. mellifera. This host shift has been

Apidologie 32 (2001) 381–394 381© INRA/DIB-AGIB/EDP Sciences, 2001

* Correspondence and reprintsE-mail: [email protected]

Original article

Resistance to the parasitic mite Varroa destructorin honey bees from far-eastern Russia

Thomas E. RINDERERa*, Lilia I. DE GUZMANa, G.T. DELATTEa,J.A. STELZERa, V.A. LANCASTERb, V. KUZNETSOVc, L. BEAMANa,

R. WATTSa, J.W. HARRISa

a USDA-ARS Honey Bee Breeding, Genetics & Physiology Laboratory, 1157 Ben Hur Road,Baton Rouge, LA 70820-5502, USA

b Neptune & Company, Inc. 1505 15th Street, Suite B, Los Alamos, NM 87544, USAc Institute of Biology and Pedology, Far East Branch of the Russian Academy of Sciences,

Vladivostok 690022, Russia

(Received 15 February 2001; revised and accepted 18 May 2001)

Abstract – Varroa destructoris a parasitic mite of the Asian honey bee, Apis cerana. Owing to hostrange expansion, it now plaguesApis mellifera, the world’s principal crop pollinator and honey pro-ducer. Evidence from A. melliferain far-eastern Russia, Primorsky (P) originating from honey beesimported in the mid 1800’s, suggested that many colonies were resistant toV. destructor. A con-trolled field study of the development of populations of V. destructorshows that P colonies have astrong, genetically based resistance to the parasite. As control colonies (D) were dying with infesta-tions of ca. 10000 mites, P colonies were surviving with infestations of ca. 4000 mites. Severalcharacteristics of the P bees contributed to suppressing the number of mites parasitizing their colonies.

Apis mellifera / mite resistance / Varrao destructor/ Russia / disease resistance / natural selection

devastating to apiculture. Apiculturists useacaricides to maintain their colonies, but arestymied by mite populations that developresistance to acaricides, and are burdenedby growing costs of controlling mites andreplacing lost colonies. Without effectiveacaricide treatments, repeated as often asthree times a year, A. melliferacolonies diefrom mite infestations. Feral and wild pop-ulations of A. mellifera, and the pollinationafforded by them, have been essentiallyeliminated in North America and Europe bythe mite (Oldroyd, 1999). While some free-living colonies continue to be discovered(Kraus and Page, 1995), they are probablyfounded by recent swarms from keptcolonies protected by acaricides.

UsingA. melliferathat are resistant toV. destructorwould greatly benefit agricul-ture and would help re-establish free-livingpopulations of honey bees. However, pro-ducing or finding suitable resistant stockshas proved daunting since most of the vari-ance in resistance in domestic Europeancolonies originates from environmental orrandom sources (Kulinclevicu et al., 1997).Starting with colonies that survived an epi-zootic of V. destructor, Kulinc levic u et al.(1992) produced a stock of honey beeswhich was only slightly more resistant thanother stocks (de Guzman et al., 1996). Harboand Harris (1999) have bred a line of beeswhich suppresses reproduction ofV. destruc-tor and may be a source of genetic resist-ance for breeding commercial stocks. How-ever, numerous breeding programs haveencountered insufficient genetic variance toproduce resistant stock.

Africanized honey bees, hybrid descen-dants of African and European honey beesimported to South America, (Rinderer et al.,1991) have been reported to be resistant toV. destructorin Brazil based on various dif-ferences from European honey bees otherthan survival (Camazine, 1986, 1988;Moretto et al., 1993; Moretto, 1997; Morettoand de Mello, 1999). However, consideringsurvival, European honey bees kept in Brazil

after importation from the United States alsoappear to be resistant (De Jong and Soares,1997) as do European honey bees inUruguay (Rosenkranz, 1999). The origin ofthe V. destructorin Brazil is Japan via neigh-boring Paraguay (de Jong et al., 1982) ratherthan Russia, the origin of the mites in most ofthe world (de Guzman et al., 1997; deGuzman et al., 1998; de Guzman andRinderer, 1999; de Guzman et al., 1999).Perhaps theV. destructorfrom Japan arehypovirulent. In any case, Africanized honeybees are undesirable for agriculture owingto their extreme defensive behavior (Collinset al., 1982), poor honey production (Rindereret al., 1984, 1985), and management diffi-culties (Danka et al., 1987), as are the report-edly resistant honey bees of Tunisia (Boeckingand Ritter, 1993). Occasionally, feralcolonies in the USA have been reported tosurvive V. destructorinfestations. However,when tested, none have been found to beresistant to V. destructor(Danka et al., 1997).

One possible source of commercially use-ful resistant European honey bees is far-eastern Russia (Primorsky) where Europeansettlers took A. melliferain the mid 1800’s(Crane, 1978). The area has native A. ceranainfested withV. destructorwhich most likelyinfested the arriving A. mellifera, resultingin the longest known association of A. mel-lifera andV. destructor(Danka et al., 1995).Preliminary examinations of A. melliferainthe Primorsky territory (P) suggested thatthey might have substantial levels of miteresistance (Danka et al., 1995). These obser-vations inspired the importation and furthertesting of a sample of P honey bee queens(Rinderer et al., 1997). An initial evaluationindicated that their commercial traits such ashoney production were similar to those ofexisting commercial stocks (Rinderer et al.,1999b). Most importantly, some of theimported P queens produced colonies whichappeared to be resistant to V. destructor(Rinderer et al., 1999b).

An experiment was undertaken to com-pare the mite population growth (MPG) of

T.E. Rinderer et al.382

V. destructorin P colonies produced bydaughter queens of resistant P queens withMPG in colonies that represented stocksused commercially in the United States (D).The goals of the experiment were to deter-mine: (1) comparative resistance, (2) if theresistance was inherited, and (3) some pos-sible mechanisms of resistance.

2. MATERIALS AND METHODS

Daughter queens were raised from prom-ising P queens imported from Russia(Rinderer et al., 1999b). Queens were col-lected within 200 km2 area north and west ofVladivostok (131°54’E 43°7’N). They weremated to drones from similar queens onGrand Terre Island, Louisiana, to assure con-trolled matings. Four stocks of commercialhoney bees were represented in theD colonies. These stocks were derivedfrom10 or more years of selection by com-mercial breeders from apiaries debilitatedby V. destructor. No further screening wasdone among the D colonies since numerousselection efforts within these stocks for vigorand production despite V. destructorhadalready occurred.

In June 1998, 22 daughter queens wereestablished in standard hives with about1.35 kg of P worker bees. The worker beescame from a common pooling which wassampled (15 subsamples washed in alcohol)to estimate the number of adult femaleV. destructorin each colony. During the firstweek the bees were in the hives, dead mitesthat fell to the floor of the hive were collectedon screen protected sticky boards, counted,and their numbers were subtracted from theinitial mite infestation of each colony, result-ing in an estimate of 305 ± 32 adult mitesper colony. Similarly, 22 queens of D stockswere established with about 1.35 kg ofD worker bees harboring about 223 ±18 mites. All the V. destructorcame fromthe current United States population ofmites: at no time have we imported livingmites from Russia.

The inequality in numbers of mitesresulted from colonies being establishedfrom two different “bulk packages”. We con-sider this technique to be the most certainway to establish precise numbers of mites inexperimental colonies. However, since onebulk package was impossible because ofsize limits, either differential numbers ofbees or differential numbers of mites at thebeginning of the experiment had to beaccepted. Since the P colonies would be dis-advantaged by having more mites but wouldbe similar to D colonies in respect to thenumber of bees, and since the experimenttested the null hypothesis that P colonieswere not more resistant to V. destructor, weselected the option which challengedP colonies with more mites.

P and D colonies were divided equallyinto two apiaries near Baton Rouge,Louisiana, with random colony placementwithin apiaries. All colonies were inspectedweekly for maintenance purposes. Theexperimental apiaries lost 6 colonies due tonon-mite related reasons during 1998 andone early in 1999 (Tab. I). These colonieswere replaced with reserve colonies estab-lished for this purpose having similar stock,histories, and mite levels. Also, followingour standard management practice, allcolonies were requeened in April 1999.When supersedure queens or queenlesscolonies were detected, the colonies wererequeened with queens of the appropriatestock (Tab. I). Supersedure queens wereunacceptable since they likely mated withmixtures of P and D drones and would pro-duce hybrid colonies. When replacementqueens were not available, the colonies wereexcluded from the remainder of the experi-ment (Tab. I). Many colonies “died” fromvarroosis (Tab. I). Some colonies were con-sidered dead when they had lost half or moreof their adult bee population, had numerousdeformed bees, had scattered and dead brood,and had at least 35% worker brood infesta-tions. The remainder of the dead colonieswere approaching these conditions theprevious month and had dwindled to no or

Resistance to Varroa destructor 383

T.E. R

inderer et al.384

Table I. Status of colonies through time showing requeening, colony replacement and loss.

Month Primorsky Domestic

unchanged re-queened replaced dead from queen loss, unchanged re-queened replaced dead from queen loss,from prior V. destructor not replaced from prior V. destructor not replaced

month month

July, 98 22 22 Aug., 98 22 22 Sept., 98 20 2 21 1 Oct., 98 20 2 20 1 1 Nov., 98 22 21 1 Dec., 99 22 21 1 Feb., 99 22 21 1 March, 99 21 1 22 April, 99 1 21 22 May, 99 22 15 7 June, 99 19 2 1 6 7 2 July, 99 16 1 3 1 4 2 Aug., 99 15 2 Sept., 99 13 2 Oct., 99 11 2 Nov., 99 11

only a very few bees when they weredeclared dead.

V. destructorpopulation dynamics wereevaluated using a comprehensive suite ofmeasurements. Each month (excepting Dec.and Jan. when cold would have damagedexposed brood), the number of adult femalemites (including nearly adult female mites)in each colony was estimated. These esti-mates were derived from: (a) counts of mitesin 200 worker brood cells (50 from eachside of two combs), (b) counts of mites in100 drone brood cells (50 from each sideof one comb or from several nest areas whendrone brood was scattered), (c) estimates ofmites per 100 adult worker bees derivedfrom counts of mites removed from 300 to600 adult worker bees by the bees beingwashed in ethanol, (d) comb by comb esti-mates (to the nearest 5%) of the numbersof sealed worker and drone brood cells inthe hive, and (e) comb by comb estimates ofthe number of bees (to the nearest 5%)

comprising the colonies. Brood samplinginvolved opening cells along a row of cellsthrough the center of the brood pattern toavoid bias resulting from the patchy distri-bution of infested cells. Mother mites andtheir daughters were individually recognizedaccording to the methods of Ifantidis (1983).

One week each month, the mites that fellto the floors of hives were collected on stickyboards. The boards were fitted with screenswhich prevented bees from biting mites afterthey were on the board. These mites wereexamined using a microscope for damageand mandible marks resulting from workerbees biting mites (grooming) (Ruttner andHänel, 1992; Boeking and Ritter, 1993).

3. RESULTS

In 1998, estimated mite populationsremained small in both groups of colonies(Fig. 1). However, the mite population


Figure 1. Average V. destructorinfestations (numbers of adult female mites) in Primorsky (black bars)and Domestic colonies (white bars) through time. Error bars = sem.

numbers showed no trend for P colonies(P = 0.72) and an increasing trend forD colonies (P= 0.003) (Gibbons, 1994). ByNov., the P colonies harbored fewer mitesthan D colonies (X y± sem (mean ± standarderror of the mean)): P = 108 ± 31, D = 395 ±93; t-test with unequal variance, P = 0.007).

In 1999, mite populations in D coloniesrose sharply (Fig. 1, Tab. II). The increase innumbers was greatest in Feb. to Mar. (4 fold)(Tab. II). The rate of increase then slowedfrom Mar. through May as numbers werereached that caused colony deaths. By May,mite populations averaged 10844 ± 1665(X y ± sem) in D colonies and 7 of theD colonies died from varroosis. After May,the average mite populations no longerincreased in D colonies since the D colonieswith the highest mite populations were dying.At the end of July, all of the D colonies weregone from the experiment. Eighteen diedfrom varroosis and four were lost becauseof queen supersedure or loss.

In comparison, the MPG in P colonieswas restricted (Tab. II, Fig. 1). The MPGwas 2.6 fold in Feb. to Mar., grew to its

highest in Mar. to Apr. (3.4 fold) and thenslowed. After July, mite populationsdecreased (Tab. II, Fig.1). During eachmonth of 1999 (Feb. to July) the number ofmites in P colonies was substantially lessthan in D colonies (allt-tests; P < 0.05) withaverages of about 6000 fewer mites in May,June and July. From July on, the averagenumbers of mites in P colonies showed adecreasing trend (P = 0.002), going fromabout 4000 in July to about 400 in Nov.Near the end of July, three P colonies died ofvarroosis with an average of 7896 mites.No other P colonies were lost from varroosis(Tab. I).

Separate data sets for the amounts ofworker brood, adult worker bees and workerbrood/adult bee ratios were analyzed as acompletely randomized design with a two-way structure (stock = P and D colonies)having 11 repeated measures over time.Although these measures changed season-ally in both P and D colonies (P < 0.05), nei-ther the stock by time interactions nor thestock main effects were significant (P > 0.35)(Fig. 2). Numbers of drone cells were ana-lyzed using a generalized linear model witha Poisson error structure. The stock by timeinteraction was not significant (P = 0.18).Both date (P = 0.0001) and stock (P = 0.02)effects were significant with P colonies hav-ing more drones (Fig. 2).

The population dynamics data from thisexperiment were further evaluated. P coloniesconsistently had a smaller percentage of theirtotal mites infesting worker brood, and alarger percentage on adult workers than didD colonies (Fig. 3; χ2 test of independence,P = 0.0001, χ2 test of heterogeneity, NS).Also, a greater proportion of mites inP colonies infested drone brood (Fig. 3;χ2 test of independence,P = 0.0001).

A greater percentage of the dead mitescollected from the P colonies had physicaldamage attributable to grooming (P = 42%(8265 of 19680 mites), D = 28% (15712of 56116 mites), χ2 test of independence,P = 0.0001, χ2 test of heterogeneity between


Table II. Month to month mite populationgrowths. Numbers less than 1 indicate popula-tion declines.

Period Primorsky Domestic colonies colonies

June 98 – July 98 0.89 1.31 July 98 – Aug. 98 0.57 1.02 Aug. 98 – Sept. 98 0.97 1.06 Sept. 98 – Oct. 98 0.94 1.08 Oct. 98 – Nov. 98 0.85 1.21 Nov. 98 – Feb. 99 1.38 2.82 Feb. 99 – Mar. 99 2.58 4.06 Mar. 99 – Apr. 99 3.39 1.75 Apr. 99 – May 99 2.36 1.32 May 99 – June 99 1.14 0.97 June 99 – July 99 0.91 0.96 July 99 – Aug. 99 0.50 – Aug. 99 – Sept. 99 0.64 – Sept. 99 – Oct. 99 0.40 – Oct. 99 – Nov. 99 0.93 –

months, NS). No seasonal variation in thesepercentages was apparent, although themonthly total of dead mites increased asinfestations grew.

The average number of mature femalemites (mothers and daughters) in infestedP worker cells was fewer than in infestedD worker cells (D = 1.87 ± 0.20, R = 1.53 ±0.27, t-test, P= 0.0001) Also, the averagenumber of adult female mites per infestedP drone cell was smaller (D = 3.14 ± 1.14,P = 2.63 ± 1.20, t-test,P = 0.0001).

4. DISCUSSION

The differences in changes in mite pop-ulations in P and D colonies and their

differential survival evidence genetic resist-ance to V. destructorby the P colonies. Theresistance is inherited since the P queenswere daughters of queens that showed a sim-ilar phenotype (Danka et al., 1995; Rindereret al., 1997, 1999b). Further, the P andD colonies shared the same experimentalenvironment including the same ecotype ofmite. Sharing the same experimental api-aries in random placement may have mutedthe observed differences since large numbersof mites were produced in dying D coloniesthat had the opportunity to enter P coloniesand mask their resistance phenotype.

The origin of the resistance appears to benumerous small differences which are bothadditive and interactive since no single


Figure 2. Box plots of total adult bees, total drone brood, total worker brood, and brood to adultbee ratios for Primorsky (P) and domestic (D) colonies from July 1998 through July 1999.● = median observation, h = range between 1st and 3rd quartile, [] = 1.5 times the interquartilerange, s = outlying observation.

overwhelming resistance mechanism wasidentified. Although they had similar workerbrood and more drone brood than D colonies,the P colonies somehow restricted the earlyseason MPG (Jan. to Mar.; Fig. 1; Tab. II)which is normally exponential (Ifantidis,1984; Schulz, 1984; Fries et al., 1994; Harboand Harris, 1999). In other periods of theyear, the P colonies had declining popula-tions of V. destructor(Tab. II). After July1999, when worker brood was still plentifuland drone brood was often present, theP colonies experienced a strong reductionin mite populations. This reduction alsooccurred in P but not in D colonies in 1998,

although to a less pronounced degree inSept. and Oct. These reductions led to muchsmaller mite populations by Nov. that weresubject to further differential attrition duringDec. and Jan. Further differential attritionin P colonies could have led to still lowermite populations and contributed to thegrowing differences in population numbersobserved in Mar. 1999. Similar “winter”attrition in colonies having brood has beenobserved in Africanized honey bees in Mex-ico (Vandame, 1996).

Several aspects of P honey bee biologymay be involved in restricting MPG. First,


Figure 3. Pie charts showingthe proportional distributionof adult female mites in Pri-morsky and domestic coloniesthrough time. Black: phoreticmites on adult bees/totalmites, white: mites infestingworker brood/total mites,gray: mites infesting dronebrood/total mites. Colonynumbers are shown for eachperiod and stock in Table I.

the greater proportions of phoretic miteswould reduce opportunities to reproduce,assuming the mites have a similar life spanin P colonies. Reproductive frequency is akey factor in MPG (de Ruijter, 1987; Otten,1991; Fries and Rosenkranz, 1993; Frieset al., 1994; Martin and Kemp, 1997) andits reduction could be a key resistance mech-anism.

Second, an increased phoretic periodincreases vulnerability to worker bee groom-ing (Büchler et al., 1992; Delfinado-Bakeret al., 1992; Bienefeld et al., 1999). Thisvulnerability seems to be exploited since adisproportionately high number of deadmites collected from P colonies show phys-ical damage attributable to grooming. Sincethe sticky boards were protected by screens,the biting occurred before the mites reachedthe sticky board. Our observed rate of bittenmites in D colonies were very similar to thatobserved inA. melliferaby Fries et al.(1996). Our rate of bitten mites in P colonieswas 1/3 higher than that observed in A. cer-anaby Fries et al. (1996).

The smaller average number of mites inboth worker and drone brood in P coloniesmight arise from differential reproductiverates or might be simply a result of P colonieshaving fewer mites and hence fewerinstances of multiple infestations (Fuchsand Langenbach, 1989). However, the sup-pression of mite reproduction hypothesisgains support from the comparison ofmonthly MPGs (Tab. II). In most months,mite populations were reduced in P colonies.Also, MPG in P colonies only exceeded thatin D colonies when D colonies were highlyinfested, dying, and unable to support furtherincreases in MPG. Additionally, field obser-vations suggest the hypothesis that the latesummer drop in mite populations is relatedto a very strong increase in non-reproductionby brood infesting mites.

The differences in resistance to V. destruc-tor did not originate from differences inworker brood, adult worker bees or workerbrood/adult bee ratios (Fries et al., 1994;

Calis et al., 1999) but occurred despiteP colonies having more drone brood. Theadditional drone brood in P colonies maylead to a tolerance effect. It may accountfor the greater proportion of mites beingfound in drone brood and reduce damage tospringtime colonies without unduly enhanc-ing MPG since reproduction appears to becomparatively less in P drone brood. Whendrone brood becomes less available in latesummer, the penetrance of the resistancephenotype is sufficient to reduce mite pop-ulations. Since this process would lead tobetter survival with more mites, it would betolerance rather than resistance.

Natural selection is the most likely causeof the heightened resistance. We are notaware of any efforts to select for resistancein the Primorsky area. Also, the mid-1800importations were prior to general use ofmovable frame hives and about 60 yearsbefore the naming of the genus Varroa(Oudemans, 1904; Crane, 1978). Lackingmovable frame hives, beekeepers could onlydivide surviving colonies or catch swarms.Founder effects are unlikely to have pro-duced resistance since the originating Ukran-ian population (or any other European honeybees) has not been reported to have anynotable resistance.

The Primorsky territory has a specific,and perhaps unique condition which mayhave fostered this selection. Although A. cer-anaand V. destructor range throughout muchof Primorsky, their occurrence is patchy(De Jong et al., 1982), perhaps because thearea is at the edge of the A. ceranarange(Ruttner, 1988). Hence, at the colony level,where infestation of worker bees indirectlyreduces reproductive fitness, the selectionby V. destructoron the importedA. melliferamay have been weak and intermittent, per-mitting marginally resistant colonies toexpress enhanced fitness via comparativelyenhanced reproduction. V. destructorpref-erentially infests drone brood (Fuchs, 1990,1992), overcoming the protection from envi-ronment afforded by the honey bee nest.Thus, weak or moderate selection at the


colony level may have been comparativelystrong on drones. If so, intense selection ondrones would accelerate selection eventhough infestation of worker bees may beinsufficient to kill the colony. V. destructorkills many infested drones and many adultdrones surviving infestation suffer severereproductive impairment (Weinberg andMadel, 1985; Del Cacho et al., 1996;Rinderer et al., 1999a). Also, since dronesare haploid, (Woyke, 1986) selection amongdrones is effectively at the gametic level,unencumbered by genetic conditions aris-ing from heterozygosity.

Overall, P honey bees appear to have sev-eral mechanisms which act in concert toprovide them with substantial resistance toV. destructor. It is unlikely that we have yetidentified all of the factors that may con-tribute to this resistance. Indeed, a substan-tial number of hypotheses remain wholly orpartially untested. However, the diversityof traits identified in this study that maycontribute to the resistance suggests that aconstellation of traits and genes underlie theoverall resistance and provide opportunitiesfor further development of the resistancethrough selective breeding.

Résumé – Résistance des abeilles domes-tiques de Russie extrême orientale à l’aca-rien Varroa destructor. En Asie V. destruc-tor est un parasite anodin d’Apis cerana.Cet acarien est passé de l’abeille asiatique àl’abeille européenne A. mellifera; il s’estrépandu rapidement et infeste maintenantla majeure partie des colonies d’A. melli-fera, causant un énorme préjudice à l’api-culture.La Russie extrême orientale (Primorsky),où les colons ont apporté Apis melliferaaumilieu du 19e siècle, constitue une sourceéventuelle de résistance à V. destructor.Nous avons importé certaines de ces abeillesaux États-Unis, où les tests ont montréqu’elles convenaient pour le commerce. Aucours d’une série d’expériences nous avonscomparé des colonies de Primorsky (P) et

des colonies locales (D) et déterminé (i) larésistance comparative, (ii) que la résistanceavait une base génétique et (iii) certainsmécanismes possibles de résistance.Des reines sœurs issues de colonies P ontété élevées, fécondées sur une île et enru-chées avec environ 305 acariens V. destruc-tor adultes. De la même façon des reinessœurs issues de colonies D ont été enru-chées avec environ 233 acariens. Nousavons évalué les populations d’acariens encomptant les acariens dans le couvain d’ou-vrière, le couvain de mâle et sur les adulteset en estimant les surfaces de couvain oper-culé et le nombre d’abeilles. Nous avonsrécolté périodiquement les acariens tombéssur le fond de la ruche et cherché des indicesde toilettage.En 1998 les populations d’acariens sont res-tées généralement faibles. Pourtant, ennovembre, les colonies P avaient moinsd’acariens (Fig. 1). En 1999 les populationsd’acariens dans les colonies D ont augmentéde façon exponentielle (Fig. 1). En mai, ellesatteignaient environ 10000 et sept des colo-nies D sont mortes de varroose. À la fin dejuillet 18 colonies D sont mortes de varrooseet quatre autres ont été perdues pour d’autresraisons. La croissance des populations d’aca-riens dans les colonies P a été fortement res-treinte (Fig. 1). Au cours de chaque mois de1999 le nombre d’acariens dans les coloniesP était nettement inférieur à celui des colo-nies D, où il atteignait environ 4000. À par-tir de juillet, le nombre moyen d’acariens amontré une tendance à la décroissance pouratteindre 400 en novembre. À la fin de juillet,trois colonies P étaient mortes de varroose.Les différences dans les populations d’aca-riens et la longévité des colonies sont despreuves de l’existence de différences géné-tiques dans la résistance à V. destructor. Larésistance est héritée puisque (i) les reinesP étaient des sœurs de reines qui présen-taient un phénotype semblable, (ii) le testcomparatif a été fait dans le même environ-nement.Les différences dans la résistance ne pro-vient pas de différences dans la quantité de


couvain d’ouvrière, d’abeilles adultes nidans les rapports couvain/adultes et exis-tent bien que les colonies P aient eu beau-coup plus de couvain de mâles (Fig. 2).Les colonies P ont eu moins d’acariens quiont infesté le couvain d’ouvrières et plusd’acariens sur les abeilles adultes. Ceci peutréduire la reproduction de la durée de vieet accroître la vulnérabilité au toilettage.Dans les colonies P un plus grand nombred’acariens tombés présentaient des lésionsdues au toilettage (P = 42 %, D = 28 %). Lenombre moyen d’acariens femelles maturesdans les cellules d’ouvrières infestéesdes colonies P était plus faible (P = 1,53 ;D = 1,87) ; ce qui suggère que le taux dereproduction de V. destructor peut être infé-rieur dans le couvain d’ouvrières des colo-nies P. De même, on a trouvé un plus grandpourcentage d’acariens dans les colonies Pinfestant le couvain de mâles (Fig. 2). Maisle nombre d’acariens par cellule de mâlesinfestée dans les colonies P était plus petit(P = 1,53 ; D = 1,87), suggérant que la repro-duction de l’acarien peut aussi être plusfaible sur le couvain de mâle des colonies P.Au total les abeilles P semblent avoir plu-sieurs mécanismes de résistance qui agis-sent de concert. Elles offrent donc des pos-sibilités de produire des lignées utilisablescommercialement qui présentent une résis-tance à V. destructor.

Apis mellifera / résistance au parasite /Varroa destructor/ Russie / résistance auxmaladies / sélection naturelle

Zusammenfassung – Resistenz gegen dieparasitische Milbe Varroa destructorinHonigbienen aus dem fernöstlichen Russ-land. Eine mögliche Fundstelle für Resis-tenz gegen V. destructorist das fernöstlicheRussland (Primorski), wohin um die Mittedes 19. Jahrhunderts Apis melliferavon Sied-lern verbracht wurde. Wir importierten einigedieser Honigbienen in die Vereinigten Staa-ten, wo ihre Überprüfung zeigte dass sie für

die kommerzielle Imkerei annehmbareEigenschaften hatten. In einem Experimentwurden Primorsky (P) und einheimische (D)Völker untersucht. Hierbei zeigte sich, dassPrimorskybienen (1) vergleichsweise resi-stent sind, (2) die Resistenz eine genetischeGrundlage hat und (3) wurden einige mög-liche Mechanismen der Resistenz bestimmt. Tochterköniginnen der P Linie wurden nach-gezogen, auf einer Insel verpaart und 22 die-ser Königinnen zusammen mit etwa 305V. destructorMilben in Völker eingesetzt.D Königinnen wurden in vergeichbarer Weisezusammen mit 223 V Milben eingeweiselt.Die Populationsgrösse von V. destructorwurde durch Zählungen von Milben inArbeiterinnenbrut, in Drohnenbrut und aufadulten Milben sowie durch Schätzungender Bienenanzahl sowie der Anzahl ver-deckelter Brutzellen bestimmt. In regelmä-ßigen Abständen wurden abgefallene Milbengesammelt und auf Anzeichen von Putz-verhalten bei den Bienen hin untersucht. 1998 blieben die Milbenpopulationen imallgemeinen niedrig. Allerdings enthieltendie P Völker im November weniger Milben(Abb. 1). 1999 wuchsen die Populationenin den D Völkern exponentiell an (Abb. 1).Im Mai waren die Populationen im Mittelauf ungefähr 10000 Milben angewachsenund 7 der D Völker gingen an der Varroosezu Grunde. Ende Juli waren 18 der D Völkeran der Varroose gestorben, 4 waren ausanderen Gründen umgekommen. DasWachstum der Milbenpopulationen in denP Völkern war stark begrenzt (Abb. 1). Inallen Monaten 1999 war die Anzahl vonVarroamilben in den P Völkern deutlichgeringer als in den D Völkern und erreichteim Mittel etwa 4000 Milben. Von Juli anzeigte die mittlere Anzahl der Milben inP Völkern eine abnehmende Tendenz undging auf etwa 400 im November zurück.Gegen Ende Juli gingen 3 der P Völker ander Varroose ein. Die Unterschiede in den Milbenpopulatio-nen und in der Lebensdauer zeigten, dassgenetische Effekte der Resistenz gegenV. destructor zu Grunde liegen. Die Resis-tenz wird vererbt: a.) die P Königinnen


waren Töchter von Königinnen einesähnlichen Phänotyps und b.) fand der Ver-gleichstest in der gleichen Umgebung statt. Die unterschiedliche Resistenz war nichtauf Unterschiede in der Erzeugung vonArbeiterinnenbrut, in den Anzahlen vonArbeiterinnen oder das Verhältnis von Brutzu Arbeiterinnen zurückzuführen, sonderntrat auf obwohl die P Völker mehr Droh-nenbrut erzeugt hatten (Abb. 2). In denP Völkern befanden sich mehr Milben aufden Arbeiterinnen und weniger in der Arbei-terinnenbrut. Dies könnte die Lebensrepro-duktionsleistung vermindern und die Ver-wundbarkeit durch das Putzverhalten derBienen erhöhen. In den P Völkern zeigtenmehr der abgefallenen Milben Verletzungendurch Putzverhalten (P = 42 %, D = 28 %).Die mittlere Anzahl ausgewachsener weib-licher Milben in den befallenen PArbeiter-innenzellen war geringer (P = 1,53, D = 1,87)was auf eine geringere Reproduktionsratevon V. destructorin P Arbeiterinnenzellenhinweist. Ebenso war der Anteil von Mil-ben in Drohnenzellen in P den Völker höher(Abb. 2). Allerdings war die Anzahl vonMilben pro befallener P Drohnenzelle gerin-ger (P = 1,53, D = 1,87). Dies könnte aufeine geringere Reproduktion in den Droh-nenzellen hinweisen. Insgesamt scheinendie P Honigbienen mehrere zusammenwir-kende Resistenzmechanismen aufzuweisen.Daher bieten P Honigbienen Möglichkeitenkommerziell verwendbare Zuchtlinien mitResistenz gegenüberV. destructorzu erstel-len.

Apis mellifera / Resistenz / Varroadestructor/ Russland / Krankheitsresis-tenz / natürliche Selektion

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