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Home , Africanized bee, Varroa destructor, Varroa jacobsoni

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

Original article

Resistance to the parasitic destructor in 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 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, USA c 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 – is a parasitic mite of the Asian , . Owing to host range expansion, it now plagues Apis mellifera, the world’s principal crop pollinator and honey pro- ducer. Evidence from A. mellifera in far-eastern Russia, Primorsky (P) originating from honey bees imported in the mid 1800’s, suggested that many colonies were resistant to V. destructor. A con- trolled field study of the development of populations of V. destructor shows that P colonies have a strong, genetically based resistance to the parasite. As control colonies (D) were dying with infesta- tions of ca. 10000 , P colonies were surviving with infestations of ca. 4000 mites. Several characteristics 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

1. INTRODUCTION shift to Apis mellifera, the that is employed world-wide for polli- In Asia, Varroa destructor Anderson and nating crops and producing honey (Boot Truman, 2000 is an innocuous external par- et al., 1997; Rath, 1999). The parasite spread asitic mite of Apis cerana, the Asian hive rapidly and now infests most the world’s bee. However, V. destructor has made a host A. mellifera. This host shift has been

* Correspondence and reprints E-mail: [email protected] 382 T.E. Rinderer et al. devastating to apiculture. Apiculturists use after importation from the also to maintain their colonies, but are appear to be resistant (De Jong and Soares, stymied by mite populations that develop 1997) as do European honey bees in resistance to acaricides, and are burdened Uruguay (Rosenkranz, 1999). The origin of by growing costs of controlling mites and the V. destructor in is Japan via neigh- replacing lost colonies. Without effective boring Paraguay (de Jong et al., 1982) rather treatments, repeated as often as than Russia, the origin of the mites in most of three times a year, A. mellifera colonies die the world (de Guzman et al., 1997; de from mite infestations. and wild pop- Guzman et al., 1998; de Guzman and ulations of A. mellifera, and the Rinderer, 1999; de Guzman et al., 1999). afforded by them, have been essentially Perhaps the V. destructor from Japan are eliminated in and Europe by hypovirulent. In any case, Africanized honey the mite (Oldroyd, 1999). While some free- bees are undesirable for agriculture owing living colonies continue to be discovered to their extreme defensive behavior (Collins (Kraus and Page, 1995), they are probably et al., 1982), poor honey production (Rinderer founded by recent swarms from kept et al., 1984, 1985), and management diffi- colonies protected by acaricides. culties (Danka et al., 1987), as are the report- edly resistant honey bees of Tunisia (Boecking Using A. mellifera that are resistant to and Ritter, 1993). Occasionally, feral V. destructor would greatly benefit agricul- colonies in the USA have been reported to ture and would help re-establish free-living survive V. destructor infestations. However, populations of honey bees. However, pro- when tested, none have been found to be ducing or finding suitable resistant stocks resistant to V. destructor (Danka et al., 1997). has proved daunting since most of the vari- ance in resistance in domestic European One possible source of commercially use- colonies originates from environmental or ful resistant European honey bees is far- random sources (Kulincevicl u et al., 1997). eastern Russia (Primorsky) where European Starting with colonies that survived an epi- settlers took A. mellifera in the mid 1800’s zootic of V. destructor, Kulincevicl u et al. (Crane, 1978). The area has native A. cerana (1992) produced a stock of honey bees infested with V. destructor which most likely which was only slightly more resistant than infested the arriving A. mellifera, resulting other stocks (de Guzman et al., 1996). Harbo in the longest known association of A. mel- and Harris (1999) have bred a line of bees lifera and V. destructor (Danka et al., 1995). which suppresses reproduction of V. destruc- Preliminary examinations of A. mellifera in tor and may be a source of genetic resist- the Primorsky territory (P) suggested that ance for breeding commercial stocks. How- they might have substantial levels of mite ever, numerous breeding programs have resistance (Danka et al., 1995). These obser- encountered insufficient genetic variance to vations inspired the importation and further produce resistant stock. testing of a sample of P honey bee queens (Rinderer et al., 1997). An initial evaluation Africanized honey bees, descen- indicated that their commercial traits such as dants of African and European honey bees honey production were similar to those of imported to , (Rinderer et al., existing commercial stocks (Rinderer et al., 1991) have been reported to be resistant to 1999b). Most importantly, some of the V. destructor in Brazil based on various dif- imported P queens produced colonies which ferences from European honey bees other appeared to be resistant to V. destructor than survival (Camazine, 1986, 1988; (Rinderer et al., 1999b). Moretto et al., 1993; Moretto, 1997; Moretto and de Mello, 1999). However, considering An experiment was undertaken to com- survival, European honey bees kept in Brazil pare the mite population growth (MPG) of Resistance to Varroa destructor 383

V. destructor in P colonies produced by The inequality in numbers of mites daughter queens of resistant P queens with resulted from colonies being established MPG in colonies that represented stocks from two different “bulk packages”. We con- used commercially in the United States (D). sider this technique to be the most certain The goals of the experiment were to deter- way to establish precise numbers of mites in mine: (1) comparative resistance, (2) if the experimental colonies. However, since one resistance was inherited, and (3) some pos- bulk package was impossible because of sible mechanisms of resistance. size limits, either differential numbers of bees or differential numbers of mites at the beginning of the experiment had to be 2. MATERIALS AND METHODS accepted. Since the P colonies would be dis- advantaged by having more mites but would Daughter queens were raised from prom- be similar to D colonies in respect to the ising P queens imported from Russia number of bees, and since the experiment (Rinderer et al., 1999b). Queens were col- tested the null hypothesis that P colonies lected within 200 km2 area north and west of were not more resistant to V. destructor, we Vladivostok (131°54’E 43°7’N). They were selected the option which challenged mated to drones from similar queens on P colonies with more mites. Grand Terre Island, , to assure con- P and D colonies were divided equally trolled matings. Four stocks of commercial into two near Baton Rouge, honey bees were represented in the Louisiana, with random colony placement D colonies. These stocks were derived within apiaries. All colonies were inspected from10 or more years of selection by com- weekly for maintenance purposes. The mercial breeders from apiaries debilitated experimental apiaries lost 6 colonies due to by V. destructor. No further screening was non-mite related reasons during 1998 and done among the D colonies since numerous one early in 1999 (Tab. I). These colonies selection efforts within these stocks for vigor were replaced with reserve colonies estab- and production despite V. destructor had lished for this purpose having similar stock, already occurred. histories, and mite levels. Also, following In June 1998, 22 daughter queens were our standard management practice, all established in standard hives with about colonies were requeened in April 1999. 1.35 kg of P worker bees. The worker bees When supersedure queens or queenless came from a common pooling which was colonies were detected, the colonies were sampled (15 subsamples washed in alcohol) requeened with queens of the appropriate to estimate the number of adult female stock (Tab. I). Supersedure queens were V. destructor in each colony. During the first unacceptable since they likely mated with week the bees were in the hives, dead mites mixtures of P and D drones and would pro- that fell to the floor of the hive were collected duce hybrid colonies. When replacement on screen protected sticky boards, counted, queens were not available, the colonies were and their numbers were subtracted from the excluded from the remainder of the experi- initial mite infestation of each colony, result- ment (Tab. I). Many colonies “died” from ing in an estimate of 305 ± 32 adult mites varroosis (Tab. I). Some colonies were con- per colony. Similarly, 22 queens of D stocks sidered dead when they had lost half or more were established with about 1.35 kg of of their adult bee population, had numerous D worker bees harboring about 223 ± deformed bees, had scattered and dead brood, 18 mites. All the V. destructor came from and had at least 35% worker brood infesta- the current United States population of tions. The remainder of the dead colonies mites: at no time have we imported living were approaching these conditions the mites from Russia. previous month and had dwindled to no or 384 T.E. Rinderer et al. not replaced V. destructor V. not replaced from prior V. destructor V. month month from prior unchanged re-queened replaced dead from queen loss, unchanged re-queened replaced dead from queen loss, Status of colonies through time showing requeening, colony replacement and loss. Month Primorsky Domestic I. Table Month Primorsky 98 July, Aug., 98 Domestic Sept., 98 Oct., 98 22 98 Nov., 22 Dec., 99 20 Feb., 99 20 March, 99 22 April, 99 22 99May, 22 21June, 99 99 July, 1 Aug., 99 2 22 Sept., 99 19 2 1 Oct., 99 16 21 99Nov., 15 13 2 11 1 11 22 22 21 3 20 21 1 21 1 21 1 22 2 1 2 1 1 1 15 2 6 22 1 7 7 4 2 2 Resistance to Varroa destructor 385 only a very few bees when they were comprising the colonies. Brood sampling declared dead. involved opening cells along a row of cells through the center of the brood pattern to V. destructor population dynamics were avoid bias resulting from the patchy distri- evaluated using a comprehensive suite of bution of infested cells. Mother mites and measurements. Each month (excepting Dec. their daughters were individually recognized and Jan. when cold would have damaged according to the methods of Ifantidis (1983). exposed brood), the number of adult female mites (including nearly adult female mites) One week each month, the mites that fell in each colony was estimated. These esti- to the floors of hives were collected on sticky mates were derived from: (a) counts of mites boards. The boards were fitted with screens in 200 worker brood cells (50 from each which prevented bees from biting mites after side of two combs), (b) counts of mites in they were on the board. These mites were 100 brood cells (50 from each side examined using a microscope for damage of one comb or from several nest areas when and mandible marks resulting from worker drone brood was scattered), (c) estimates of bees biting mites (grooming) (Ruttner and mites per 100 adult worker bees derived Hänel, 1992; Boeking and Ritter, 1993). from counts of mites removed from 300 to 600 adult worker bees by the bees being washed in ethanol, (d) comb by comb esti- 3. RESULTS mates (to the nearest 5%) of the numbers of sealed worker and drone brood cells in In 1998, estimated mite populations the hive, and (e) comb by comb estimates of remained small in both groups of colonies the number of bees (to the nearest 5%) (Fig. 1). However, the mite population

Figure 1. Average V. destructor infestations (numbers of adult female mites) in Primorsky (black bars) and Domestic colonies (white bars) through time. Error bars = sem. 386 T.E. Rinderer et al.

Table II. Month to month mite population highest in Mar. to Apr. (3.4 fold) and then growths. Numbers less than 1 indicate popula- slowed. After July, mite populations tion declines. decreased (Tab. II, Fig.1). During each Period Primorsky Domestic month of 1999 (Feb. to July) the number of colonies colonies mites in P colonies was substantially less than in D colonies (all t-tests; P < 0.05) with June 98 – July 98 0.89 1.31 averages of about 6000 fewer mites in May, July 98 – Aug. 98 0.57 1.02 June and July. From July on, the average Aug. 98 – Sept. 98 0.97 1.06 numbers of mites in P colonies showed a Sept. 98 – Oct. 98 0.94 1.08 decreasing trend (P = 0.002), going from Oct. 98 – Nov. 98 0.85 1.21 about 4000 in July to about 400 in Nov. Nov. 98 – Feb. 99 1.38 2.82 Feb. 99 – Mar. 99 2.58 4.06 Near the end of July, three P colonies died of Mar. 99 – Apr. 99 3.39 1.75 varroosis with an average of 7896 mites. Apr. 99 – May 99 2.36 1.32 No other P colonies were lost from varroosis May 99 – June 99 1.14 0.97 (Tab. I). June 99 – July 99 0.91 0.96 Separate data sets for the amounts of July 99 – Aug. 99 0.50 – Aug. 99 – Sept. 99 0.64 – worker brood, adult worker bees and worker Sept. 99 – Oct. 99 0.40 – brood/adult bee ratios were analyzed as a Oct. 99 – Nov. 99 0.93 – completely randomized design with a two- way structure (stock = P and D colonies) having 11 repeated measures over time. Although these measures changed season- numbers showed no trend for P colonies ally in both P and D colonies (P < 0.05), nei- (P = 0.72) and an increasing trend for ther the stock by time interactions nor the D colonies (P = 0.003) (Gibbons, 1994). By stock main effects were significant (P > 0.35) Nov., the P colonies harbored fewer mites (Fig. 2). Numbers of drone cells were ana- than D colonies (X y± sem (mean ± standard lyzed using a generalized linear model with error of the mean)): P = 108 ± 31, D = 395 ± a Poisson error structure. The stock by time 93; t-test with unequal variance, P = 0.007). interaction was not significant (P = 0.18). Both date (P = 0.0001) and stock (P = 0.02) In 1999, mite populations in D colonies effects were significant with P colonies hav- rose sharply (Fig. 1, Tab. II). The increase in ing more drones (Fig. 2). numbers was greatest in Feb. to Mar. (4 fold) (Tab. II). The rate of increase then slowed The population dynamics data from this from Mar. through May as numbers were experiment were further evaluated. P colonies reached that caused colony deaths. By May, consistently had a smaller percentage of their mite populations averaged 10844 ± 1665 total mites infesting worker brood, and a (X y ± sem) in D colonies and 7 of the larger percentage on adult workers than did D colonies died from varroosis. After May, D colonies (Fig. 3; χ2 test of independence, the average mite populations no longer P = 0.0001, χ2 test of heterogeneity, NS). increased in D colonies since the D colonies Also, a greater proportion of mites in with the highest mite populations were dying. P colonies infested drone brood (Fig. 3; At the end of July, all of the D colonies were χ2 test of independence, P = 0.0001). gone from the experiment. Eighteen died A greater percentage of the dead mites from varroosis and four were lost because collected from the P colonies had physical of queen supersedure or loss. damage attributable to grooming (P = 42% In comparison, the MPG in P colonies (8265 of 19680 mites), D = 28% (15712 was restricted (Tab. II, Fig. 1). The MPG of 56116 mites), χ2 test of independence, was 2.6 fold in Feb. to Mar., grew to its P = 0.0001, χ2 test of heterogeneity between Resistance to Varroa destructor 387

Figure 2. Box plots of total adult bees, total drone brood, total worker brood, and brood to adult bee ratios for Primorsky (P) and domestic (D) colonies from July 1998 through July 1999. ● = median observation, ᮀ = range between 1st and 3rd quartile, [] = 1.5 times the interquartile range, ᭺ = outlying observation. months, NS). No seasonal variation in these differential survival evidence genetic resist- percentages was apparent, although the ance to V. destructor by the P colonies. The monthly total of dead mites increased as resistance is inherited since the P queens infestations grew. were daughters of queens that showed a sim- The average number of mature female ilar phenotype (Danka et al., 1995; Rinderer mites (mothers and daughters) in infested et al., 1997, 1999b). Further, the P and P worker cells was fewer than in infested D colonies shared the same experimental D worker cells (D = 1.87 ± 0.20, R = 1.53 ± environment including the same ecotype of 0.27, t-test, P= 0.0001) Also, the average mite. Sharing the same experimental api- number of adult female mites per infested aries in random placement may have muted P drone cell was smaller (D = 3.14 ± 1.14, the observed differences since large numbers P = 2.63 ± 1.20, t-test, P = 0.0001). of mites were produced in dying D colonies that had the opportunity to enter P colonies and mask their resistance phenotype. 4. DISCUSSION The origin of the resistance appears to be The differences in changes in mite pop- numerous small differences which are both ulations in P and D colonies and their additive and interactive since no single 388 T.E. Rinderer et al.

Figure 3. Pie charts showing the proportional distribution of adult female mites in Pri- morsky and domestic colonies through time. Black: phoretic mites on adult bees/total mites, white: mites infesting worker brood/total mites, gray: mites infesting drone brood/total mites. Colony numbers are shown for each period and stock in Table I.

overwhelming resistance mechanism was although to a less pronounced degree in identified. Although they had similar worker Sept. and Oct. These reductions led to much brood and more drone brood than D colonies, smaller mite populations by Nov. that were the P colonies somehow restricted the early subject to further differential attrition during season MPG (Jan. to Mar.; Fig. 1; Tab. II) Dec. and Jan. Further differential attrition which is normally exponential (Ifantidis, in P colonies could have led to still lower 1984; Schulz, 1984; Fries et al., 1994; Harbo mite populations and contributed to the and Harris, 1999). In other periods of the growing differences in population numbers year, the P colonies had declining popula- observed in Mar. 1999. Similar “winter” tions of V. destructor (Tab. II). After July attrition in colonies having brood has been 1999, when worker brood was still plentiful observed in Africanized honey bees in Mex- and drone brood was often present, the ico (Vandame, 1996). P colonies experienced a strong reduction in mite populations. This reduction also Several aspects of P honey bee biology occurred in P but not in D colonies in 1998, may be involved in restricting MPG. First, Resistance to Varroa destructor 389 the greater proportions of phoretic mites Calis et al., 1999) but occurred despite would reduce opportunities to reproduce, P colonies having more drone brood. The assuming the mites have a similar life span additional drone brood in P colonies may in P colonies. Reproductive frequency is a lead to a tolerance effect. It may account key factor in MPG (de Ruijter, 1987; Otten, for the greater proportion of mites being 1991; Fries and Rosenkranz, 1993; Fries found in drone brood and reduce damage to et al., 1994; Martin and Kemp, 1997) and springtime colonies without unduly enhanc- its reduction could be a key resistance mech- ing MPG since reproduction appears to be anism. comparatively less in P drone brood. When drone brood becomes less available in late Second, an increased phoretic period summer, the penetrance of the resistance increases vulnerability to groom- phenotype is sufficient to reduce mite pop- ing (Büchler et al., 1992; Delfinado-Baker ulations. Since this process would lead to et al., 1992; Bienefeld et al., 1999). This better survival with more mites, it would be vulnerability seems to be exploited since a tolerance rather than resistance. disproportionately high number of dead mites collected from P colonies show phys- Natural selection is the most likely cause ical damage attributable to grooming. Since of the heightened resistance. We are not the sticky boards were protected by screens, aware of any efforts to select for resistance the biting occurred before the mites reached in the Primorsky area. Also, the mid-1800 the sticky board. Our observed rate of bitten importations were prior to general use of mites in D colonies were very similar to that movable frame hives and about 60 years observed in A. mellifera by Fries et al. before the naming of the genus Varroa (1996). Our rate of bitten mites in P colonies (Oudemans, 1904; Crane, 1978). Lacking was 1/3 higher than that observed in A. cer- movable frame hives, beekeepers could only ana by Fries et al. (1996). divide surviving colonies or catch swarms. Founder effects are unlikely to have pro- The smaller average number of mites in duced resistance since the originating Ukran- both worker and drone brood in P colonies ian population (or any other European honey might arise from differential reproductive bees) has not been reported to have any rates or might be simply a result of P colonies notable resistance. having fewer mites and hence fewer instances of multiple infestations (Fuchs The Primorsky territory has a specific, and Langenbach, 1989). However, the sup- and perhaps unique condition which may pression of mite reproduction hypothesis have fostered this selection. Although A. cer- gains support from the comparison of ana and V. destructor range throughout much monthly MPGs (Tab. II). In most months, of Primorsky, their occurrence is patchy mite populations were reduced in P colonies. (De Jong et al., 1982), perhaps because the Also, MPG in P colonies only exceeded that area is at the edge of the A. cerana range in D colonies when D colonies were highly (Ruttner, 1988). Hence, at the colony level, infested, dying, and unable to support further where infestation of worker bees indirectly increases in MPG. Additionally, field obser- reduces reproductive fitness, the selection by V. destructor on the imported A. mellifera vations suggest the hypothesis that the late may have been weak and intermittent, per- summer drop in mite populations is related mitting marginally resistant colonies to to a very strong increase in non-reproduction express enhanced fitness via comparatively by brood infesting mites. enhanced reproduction. V. destructor pref- The differences in resistance to V. destruc- erentially infests drone brood (Fuchs, 1990, tor did not originate from differences in 1992), overcoming the protection from envi- worker brood, adult worker bees or worker ronment afforded by the honey bee nest. brood/adult bee ratios (Fries et al., 1994; Thus, weak or moderate selection at the 390 T.E. Rinderer et al. colony level may have been comparatively des colonies locales (D) et déterminé (i) la strong on drones. If so, intense selection on résistance comparative, (ii) que la résistance drones would accelerate selection even avait une base génétique et (iii) certains though infestation of worker bees may be mécanismes possibles de résistance. insufficient to kill the colony. V. destructor Des reines sœurs issues de colonies P ont kills many infested drones and many adult été élevées, fécondées sur une île et enru- drones surviving infestation suffer severe chées avec environ 305 acariens V. destruc- reproductive impairment (Weinberg and tor adultes. De la même façon des reines Madel, 1985; Del Cacho et al., 1996; sœurs issues de colonies D ont été enru- Rinderer et al., 1999a). Also, since drones chées avec environ 233 acariens. Nous are haploid, (Woyke, 1986) selection among avons évalué les populations d’acariens en drones is effectively at the gametic level, comptant les acariens dans le couvain d’ou- unencumbered by genetic conditions aris- vrière, le couvain de mâle et sur les adultes ing from heterozygosity. et en estimant les surfaces de couvain oper- Overall, P honey bees appear to have sev- culé et le nombre d’abeilles. Nous avons eral mechanisms which act in concert to récolté périodiquement les acariens tombés provide them with substantial resistance to sur le fond de la ruche et cherché des indices V. destructor. It is unlikely that we have yet de toilettage. identified all of the factors that may con- En 1998 les populations d’acariens sont res- tribute to this resistance. Indeed, a substan- tées généralement faibles. Pourtant, en tial number of hypotheses remain wholly or novembre, les colonies P avaient moins partially untested. However, the diversity d’acariens (Fig. 1). En 1999 les populations of traits identified in this study that may d’acariens dans les colonies D ont augmenté contribute to the resistance suggests that a de façon exponentielle (Fig. 1). En mai, elles constellation of traits and genes underlie the atteignaient environ 10000 et sept des colo- overall resistance and provide opportunities nies D sont mortes de varroose. À la fin de for further development of the resistance juillet 18 colonies D sont mortes de varroose through selective breeding. et quatre autres ont été perdues pour d’autres raisons. La croissance des populations d’aca- riens dans les colonies P a été fortement res- Résumé – Résistance des abeilles domes- treinte (Fig. 1). Au cours de chaque mois de tiques de Russie extrême orientale à l’aca- 1999 le nombre d’acariens dans les colonies rien Varroa destructor. En Asie V. destruc- P était nettement inférieur à celui des colo- tor est un parasite anodin d’Apis cerana. nies D, où il atteignait environ 4000. À par- Cet acarien est passé de l’abeille asiatique à tir de juillet, le nombre moyen d’acariens a l’abeille européenne A. mellifera ; il s’est montré une tendance à la décroissance pour répandu rapidement et infeste maintenant atteindre 400 en novembre. À la fin de juillet, la majeure partie des colonies d’A. melli- trois colonies P étaient mortes de varroose. fera, causant un énorme préjudice à l’api- Les différences dans les populations d’aca- culture. riens et la longévité des colonies sont des La Russie extrême orientale (Primorsky), preuves de l’existence de différences géné- où les colons ont apporté Apis mellifera au tiques dans la résistance à V. destructor. La milieu du 19e siècle, constitue une source résistance est héritée puisque (i) les reines éventuelle de résistance à V. destructor. P étaient des sœurs de reines qui présen- Nous avons importé certaines de ces abeilles taient un phénotype semblable, (ii) le test aux États-Unis, où les tests ont montré comparatif a été fait dans le même environ- qu’elles convenaient pour le commerce. Au nement. cours d’une série d’expériences nous avons Les différences dans la résistance ne pro- comparé des colonies de Primorsky (P) et vient pas de différences dans la quantité de Resistance to Varroa destructor 391 couvain d’ouvrière, d’abeilles adultes ni die kommerzielle Imkerei annehmbare dans les rapports couvain/adultes et exis- Eigenschaften hatten. In einem Experiment tent bien que les colonies P aient eu beau- wurden Primorsky (P) und einheimische (D) coup plus de couvain de mâles (Fig. 2). Völker untersucht. Hierbei zeigte sich, dass Les colonies P ont eu moins d’acariens qui Primorskybienen (1) vergleichsweise resi- ont infesté le couvain d’ouvrières et plus stent sind, (2) die Resistenz eine genetische d’acariens sur les abeilles adultes. Ceci peut Grundlage hat und (3) wurden einige mög- réduire la reproduction de la durée de vie liche Mechanismen der Resistenz bestimmt. et accroître la vulnérabilité au toilettage. Tochterköniginnen der P Linie wurden nach- Dans les colonies P un plus grand nombre gezogen, auf einer Insel verpaart und 22 die- d’acariens tombés présentaient des lésions ser Königinnen zusammen mit etwa 305 dues au toilettage (P = 42 %, D = 28 %). Le V. destructor Milben in Völker eingesetzt. nombre moyen d’acariens femelles matures D Königinnen wurden in vergeichbarer Weise dans les cellules d’ouvrières infestées zusammen mit 223 V Milben eingeweiselt. des colonies P était plus faible (P = 1,53 ; Die Populationsgrösse von V. destructor D = 1,87) ; ce qui suggère que le taux de wurde durch Zählungen von Milben in reproduction de V. destructor peut être infé- Arbeiterinnenbrut, in Drohnenbrut und auf rieur dans le couvain d’ouvrières des colo- adulten Milben sowie durch Schätzungen nies P. De même, on a trouvé un plus grand der Bienenanzahl sowie der Anzahl ver- pourcentage d’acariens dans les colonies P deckelter Brutzellen bestimmt. In regelmä- infestant le couvain de mâles (Fig. 2). Mais ßigen Abständen wurden abgefallene Milben le nombre d’acariens par cellule de mâles gesammelt und auf Anzeichen von Putz- infestée dans les colonies P était plus petit verhalten bei den Bienen hin untersucht. (P = 1,53 ; D = 1,87), suggérant que la repro- 1998 blieben die Milbenpopulationen im duction de l’acarien peut aussi être plus allgemeinen niedrig. Allerdings enthielten faible sur le couvain de mâle des colonies P. die P Völker im November weniger Milben Au total les abeilles P semblent avoir plu- (Abb. 1). 1999 wuchsen die Populationen sieurs mécanismes de résistance qui agis- in den D Völkern exponentiell an (Abb. 1). sent de concert. Elles offrent donc des pos- Im Mai waren die Populationen im Mittel sibilités de produire des lignées utilisables auf ungefähr 10000 Milben angewachsen commercialement qui présentent une résis- und 7 der D Völker gingen an der Varroose tance à V. destructor. zu Grunde. Ende Juli waren 18 der D Völker an der Varroose gestorben, 4 waren aus anderen Gründen umgekommen. Das Apis mellifera / résistance au parasite / Wachstum der Milbenpopulationen in den Varroa destructor / Russie / résistance aux P Völkern war stark begrenzt (Abb. 1). In maladies / sélection naturelle allen Monaten 1999 war die Anzahl von Varroamilben in den P Völkern deutlich geringer als in den D Völkern und erreichte im Mittel etwa 4000 Milben. Von Juli an Zusammenfassung – Resistenz gegen die zeigte die mittlere Anzahl der Milben in parasitische Milbe Varroa destructor in P Völkern eine abnehmende Tendenz und Honigbienen aus dem fernöstlichen Russ- ging auf etwa 400 im November zurück. land. Eine mögliche Fundstelle für Resis- Gegen Ende Juli gingen 3 der P Völker an tenz gegen V. destructor ist das fernöstliche der Varroose ein. Russland (Primorski), wohin um die Mitte Die Unterschiede in den Milbenpopulatio- des 19. Jahrhunderts Apis mellifera von Sied- nen und in der Lebensdauer zeigten, dass lern verbracht wurde. Wir importierten einige genetische Effekte der Resistenz gegen dieser Honigbienen in die Vereinigten Staa- V. destructor zu Grunde liegen. Die Resis- ten, wo ihre Überprüfung zeigte dass sie für tenz wird vererbt: a.) die P Königinnen 392 T.E. Rinderer et al. waren Töchter von Königinnen eines Boecking O., Ritter W. (1993) Grooming and removal ähnlichen Phänotyps und b.) fand der Ver- behaviour of Apis mellifera intermissa in Tunisia against , J. Apic. Res. 32, 127–134. gleichstest in der gleichen Umgebung statt. Boot W.J., Nguyen Q.T., Pham C.D., Luong V.H., Die unterschiedliche Resistenz war nicht Nguyen V.D., Le T.L., Beetsma J. (1997) Repro- auf Unterschiede in der Erzeugung von ductive success of Varroa jacobsoni in brood of its Arbeiterinnenbrut, in den Anzahlen von original host, Apis cerana, in comparison to that of its new host, A. mellifera (: Api- Arbeiterinnen oder das Verhältnis von Brut dae), Bull. Entomol. Res. 87, 119–126. zu Arbeiterinnen zurückzuführen, sondern Büchler R., Drescher W., Tornier I. (1992) Grooming trat auf obwohl die P Völker mehr Droh- behaviour of Apis cerana, Apis mellifera and Apis nenbrut erzeugt hatten (Abb. 2). In den dorsata and its effects on the parasitic mites Varroa P Völkern befanden sich mehr Milben auf jacobsoni and Tropilaelaps clareae, Exp. Appl. Acarol. 16, 313–319. den Arbeiterinnen und weniger in der Arbei- Calis J.N.M., Fries I., Ryrie S.C. (1999) Population terinnenbrut. Dies könnte die Lebensrepro- modeling of Varroa jacobsoni, Apidologie 30, duktionsleistung vermindern und die Ver- 111–124. wundbarkeit durch das Putzverhalten der Camazine S. (1986) Differential reproduction of the Bienen erhöhen. In den P Völkern zeigten mite, Varroa jacobsoni (: Varroidae) on Africanized and European honey bees mehr der abgefallenen Milben Verletzungen (Hymenoptera: Apidae), Ann. Entomol. Soc. Am. durch Putzverhalten (P = 42 %, D = 28 %). 79, 801–803. Die mittlere Anzahl ausgewachsener weib- Camazine S. (1988) Factors affecting the severity of licher Milben in den befallenen P Arbeiter- Varroa jacobsoni infestations on European and innenzellen war geringer (P = 1,53, D = 1,87) Africanized honey bees, in: Needham G.R., Page R.E. Jr., Delfinado-Baker M., Bowman C.E. (Eds.), was auf eine geringere Reproduktionsrate Africanized honey bees and bee mites, E. Horwood von V. destructor in P Arbeiterinnenzellen Ltd./Halsted Press, New York, pp. 444–451. hinweist. Ebenso war der Anteil von Mil- Collins A.M., Rinderer T.E., Harbo J.R., Bolten A.B. ben in Drohnenzellen in P den Völker höher (1982) Colony defense by Africanized and Euro- (Abb. 2). 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