Reproduction of Varroa jacobsoni in colonies of Apis cerana indica under natural and experimental conditions Nc Tewarson, A Singh, W Engels

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Nc Tewarson, A Singh, W Engels. Reproduction of Varroa jacobsoni in colonies of Apis cerana indica under natural and experimental conditions. Apidologie, Springer Verlag, 1992, 23 (2), pp.161-171. ￿hal-00890982￿

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Reproduction of Varroa jacobsoni in colonies of Apis cerana indica under natural and experimental conditions

NC Tewarson1 A Singh W Engels

1 Ewing Christian College, Department of Zoology, Allahabad 211003, India; 2 Zoologisches Institut der Universität Tübingen, Auf der Morgenstelle 28, D-7400 Tübingen, Germany

(Received 11 March 1991; accepted 11 February 1992)

Summary — In North India the infestation with Varroa jacobsoni of drone and worker brood in Apis cerana colonies was checked monthly. Natural reproduction of the mite was found to be restricted to drone brood and to springtime. The potential reproduction in worker brood was investigated by artifi- cially induced infection. Since the bees recognized and eliminated any mites originating from other hives, the grafting was performed within the same colony. Even then, 75% of the transferred mites were removed by the bees. Of the remaining Varroa females, about 90% were found to be infertile. The significance of the hitherto known varroatosis resistance factors related to reproduction is dis- cussed with regard to a balanced host-parasite relationship.

Apis cerana indica / Varroa jacobsoni / reproduction I female mite infertility / varroatosis re- sistance

INTRODUCTION 1986). However, this could not be con- firmed by a recent titer study using radio- The host-parasite relationships between immunoassay techniques (Rosenkranz et data on the hor- the eastern honey bee, Apis cerana, and al, 1990). Comparable the mite, Varroa jacobsoni, has not been mone titer in Apis cerana larvae are lack- sufficiently studied. Several observations ing. Therefore the question of why Varroa succeeds on drone suggest that low reproduction of the para- reproduction only brood in cerana bees remains site in worker brood plays an important open. role in varroatosis resistance of Apis cera- Since higher parasitization of drone na (Koeniger et al, 1981; Tewarson, 1987; brood in both the original host, Apis cera- de Jong, 1988). Female mite fertility was na (Koeniger et al, 1983; Tewarson, 1987; presumed to be regulated by the level of de Jong, 1988), and the secondary host, juvenile hormone present in the hemo- Apis mellifera (Sulimanovic et al, 1982; lymph of its host, particularly of late 5th in- Engels et al, 1984; Issa and Gonçalves, star bee larvae (Hänel and Koeniger, 1984; Schulz, 1984; Rosenkranz and En- gels, 1985; Fuchs, 1990) is well document- Beekeeping at Allahabad ed, one possible explanation might be that, in the case of the eastern bee, honey Beekeepers multiply Apis cerana indica colonies reproductive mites avoid worker brood be- by division and also try to catch swarms. There cause of the low probability to survive. If is no queen-rearing practised in the Allahabad introduced they could perhaps become fer- region. Therefore, the local bee population con- tile in this microhabitat. sists of a mixture of hived and feral colonies. Many beekeepers have only 2 or 3 colonies, In order to test this we hypothesis, and large apiaries are found mainly in the moun- transferred reproductive Varroa females tain areas of Uttar Pradesh state. The average between already capped drone and worker annual honey yield per colony is about 2.5-4.5 brood cells of Apis cerana. Because pre- kg. Varroatosis in the eastern honey bee does liminary observations indicated that the not require any control measures. bees easily recognize any alien mites, the transfer was carried out within the same colony. The reproductive success of such Experimental colonies grafted mites was checked about a week later. The experiments were carried out in Experimental colonies of Apis cerana indica India during the early spring breeding sea- were maintained on the campus of Ewing Chris- son. At the same time the rate of natural tian College, Allahabad. The wooden hives con- brood infestation was checked. tained 8 brood frames measuring 28 x 18 cm and a super 28 x 9 cm with the same number of honey frames. For 2 naturally built brood combs the number of cells per square unit of each was MATERIALS AND METHODS determined. We counted 423-446 cells per 100 cm2 for the drone combs and 660-693 for the worker combs. of the within Timing experiments For the experiments 10 strong colonies with the annual colony cycle in North India a minimum of 5 covered brood combs and plen- ty of drone brood were selected. Only healthy At Allahabad, spring begins in late January. At colonies without sacbrood or other infections were used. To the colonies in condi- this time, a rise in brood rearing can be ob- keep good served in all Apis cerana indica colonies. tion, syrup was given from July through Septem- Swarming occurs in March and April. Drones ber and again from mid-November through mid- are usually present from February until mid- January. About 2 kg of sugar was fed per colo- May. In the hot month of June adult drones dis- ny. appear in many colonies, and in July the brood nest becomes small. The monsoon rain begins at the end of June or the first half of July. During Control of natural Varroa infestation the monsoon season there is little nectar flow, and the colonies fade. Rain terminates in Au- gust, but forage is scarce until the end of Sep- Natural brood infestation by Varroa jacobsoni tember. In October and November during the was checked throughout the year in the experi- fall blossom, the colonies are stimulated to mental colonies. Twice a month 100 sealed breed again. In December, brood rearing is worker and, if available, the same number of largely interrupted by the brief winter cold. drone brood cells per hive were opened and in- Hence at Allahabad, brood is present through- spected for mites. In all colonies Varroa jacob- out the year, and in strong colonies some drone soni was present all times, but no visible hazard larvae may be found at any time. The best peri- was recorded. Corresponding observations od for experiments requiring abundant drone have been made since we began our varroato- brood, however, is early springtime. sis research project in 1984. Artificial infection of worker broad nies 6-8% of the sealed worker cells were infested. One and occasionally even 2 fe- male mites were All these Varroa The experiments were conducted from January present. females were since no through April in 1988 and 1989. Out of the 10 ex- apparently infertile, perimental hives, 1-3 at a time were randomly eggs or nymphs were detected in worker used per transfer day, resulting in a total of 42 cells. at 24 dates Indi- within-colony graftings (table II). the which lasted vidual brood cells were marked by means of a During experiments, the rate of transparent sheet. For grafting, Varroa jacobsoni from January through April, females were removed from recently capped drone brood infestation varied considera- drone cells. In a transfer experiment, 12-15 fe- bly among the 10 hives and over the male mites were collected within 10-15 min and course of the season (table I). The range stored in a Petri dish on wet paper. Only suppos- was from 0-54.0% in 1988 and from 1.5- mites with swollen opisthosoma edly reproductive 60.5% in 1989. The monthly mean per- were taken. A small opening in the capping of a of infested drone brood cells was freshly sealed worker brood cell was made with centage and 34.0% 1988 the forceps. A mite was positioned at the end of a between 5.1 (fig 1). In needle and introduced into the cell. The cell was peak of drone brood parasitization was then sealed again using a hot needle. This graft- reached in March; and in 1989 already by ing was carried out within the same colony, be- February, but which continued in March. In cause we had observed in preliminary experi- 1989 the level of infestation was ments that the bees and higher easily recognized than in 1988. Similar fluctuations had been removed mites originating from other colonies, in particular if collected in Apis mellifera hives. Eight recorded in previous years. In the spring to 10 days later, the artificially infected cells were periods, practically all female mites in opened and inspected for a normally developed host pupa and the presence of a female mite and eggs. Over the 2 spring seasons, a total of more than 400 female mites were transferred.

RESULTS

Natural colony infestation

January through May, during the drone brood and swarming season, only very few worker cells were found to contain female mites. The maximum infestation constitut- ing less than 1% was usually observed in March. At this time the ratio of parasitized worker and drone brood cells was approxi- mately 1:30. However, during the rainy season, particularly from mid-June through mid-September, a number of Varroa fe- males were found to have invaded the worker brood. Then the brood nest was re- duced to 1 or 2 combs, and little or no drone brood was available. In some colo- drone brood were found to be fertile, with DISCUSSION the exception of some cells which were in- vaded a number of times. There was no in- dication of frequent uncapping and re- Artificial infestation moval of Varroa-infested drone larvae.

We cannot exclude the possibility that in Transfer experiments our experiments the manipulations had some negative effect on the grafted Varroa females. With one exception, the few fertile after Eight-10 days within-colony grafting mites laid only one egg, and no hatched of invaded and hence already reproductive nymphs were found. However, in Europe Varroa females from capped drone into and also in Brazil, similar transfers did not worker brood 75% of these mites cells, result in increased removal, mortality or in- had disappeared (table II). Nevertheless, fertility of the mites (Rosenkranz, 1990a, b). most of the infested worker cells artificially Experiments are scheduled in which we were found sealed and properly containing will attempt to answer this question for ce- a at the pupa expected stage. Apparently, rana bees by within-colony transfer be- the bees had merely removed the para- tween drone cells using the technique de- sites. Of approximately 25% of mites scribed here, and also by sham-transfers which were recovered live, only a few had and modified methods. laid eggs, which equals 3% of all the graft- ed Varroa females. In other words, approx- 90% of the transferred mites sur- imately Mite viving in worker brood remained infertile. fertility This is not very different from the 100% in- fertility observed in the Varroa females Although in colonies of Apis cerana indica which had naturally invaded worker brood Varroa jacobsoni females were found to in- cells. vade not only drone but also worker brood cells, reproduction of the parasite was re- sult in normal fertility of the mites surviving stricted to drone hosts. A significant sea- in experimentally-infected worker brood sonal dependence of the reproductive suc- cells. Only about 10% of the transferred cess in drone brood was described earlier and surviving Varroa females laid an egg. (Tewarson, 1987). Therefore, all the trans- Hence the pronounced infestation of drone fer experiments were conducted during brood in Apis cerana colonies is not the early springtime when virtually 100% of the only reason for the lack of Varroa repro- Varroa females, once they had entered duction in worker brood. Whether the re- drone cells, could be expected to become stricted parasitization of worker larvae is fertile. However, these graftings did not re- caused primarily by a high preference of drone hosts by the female mites invading since in the free-built cerana combs drone brood cells prior to operculation (Tewar- cells are always around the lower margin. son, 1986), or whether it is a secondary ef- Data on the exact temperature regime in fect depending on the behavior of the adult the nest of Apis cerana are still lacking. bees is as yet unknown and should be evaluated by an in vitro bioassay (Rosen- kranz et al, 1984). Hygienic behavior Host-dependent conditions evidently determine the striking differences in the The disappearance of artificially-introduced mites’ reproductive success in drone and mites from sealed worker brood cells was worker brood. A similar infertility of Varroa also recently recorded by Rath and Dres- females in 50-60% of the worker brood cher (1990) working with Apis cerana in cells of Africanized mellifera colonies Apis Thailand. The cells are probably opened was described in Brazil and de (Ritter by the bees, and the Varroa females are Jong, 1984; Camazine, 1986; Rosenkranz removed or leave on their own accord. Moretto and found et al, 1990; et al, 1991) Thereafter the bees may seal the brood to correspond with tolerance to varroato- cells again, and the worker larvae develop sis. A worker-specific influence on mite fer- normally. We did not observe the bees do- tility was similarly observed in colonies of ing this, but the fact that 8-10 days later different races of mellifera in South Apis many cells did contain pupae of the ex- America et et (Ruttner al, 1984; Engels al, pected age but no mites requires interpre- 1986; Rosenkranz, 1990a) and Europe tation. Of course, direct visual control of (Sulimanovic et al, 1986). It must be con- the involved behavior of the brood- cluded that a low of percentage ovipositing attending adult worker bees by means of Varroa mites in worker brood cells is an an observation hive is desirable. In con- trait of bee colonies re- important honey trast to our results, in Thailand nearly all sistant to varroatosis. Apparently the titer worker cells into which live or dead mites of hormone in the of juvenile hemolymph had been placed were uncapped, and the the host larva et (Rosenkranz al, 1990) mites and the bee larvae / pupae were al- does not the of the regulate reproduction ways removed. In a few experiments with female parasite, as suggested earlier dead mites these bodies were taken out and (Hänel Koeniger, 1986). and the brood was sealed again as in our Of course Varroa infertility in worker graftings. The differences are probably due brood of Apis cerana could also depend on to olfactory detection of the introduced environmental conditions. For instance, the mites by the cerana workers in Thailand cappings of drone brood cells are naturally since all the Varroa females had been col- perforated (Hänel and Ruttner, 1985; Oka- lected from A mellifera colonies. We had da, 1990) and may faciliate gaseous ex- observed in preliminary experiments that change and thereby influence relative hu- mites sampled in other colonies, in particu- midity as well as CO2 partial pressure lar of A mellifera, were rapidly recognized inside the sealed cell (Abbas and Engels, and removed by A c indica worker bees af- 1989; Chiesa et al, 1989). However, in Apis ter artificial infestation. For that reason, we mellifera the Varroa mites are fertile in carried out all subsequent experimental worker and drone brood cells without cap- mite introductions into capped worker pings. Local comb temperature (Le Conte brood cells as within-colony grafts. Never- and Arnold, 1989) may also play a role theless, about 75% of our transferred mites were not recovered. The removal of moved from infested worker than from Varroa in response to their artifical intro- drone brood (Koeniger, 1987; Rath and duction to worker brood was likewise ob- Drescher, 1990). Varroa infertility in worker served in A mellifera colonies (Boecking brood is undoubtedly another important and Drescher, 1991). Again, mites from factor of resistance towards varroatosis in other colonies and, in addition, plastic this species (de Jong, 1988) and was like- combs were used which might have influ- wise observed in the Africanized Apis mel- enced the hygienic behavior of the work- lifera from Brazil (Ritter and de Jong, 1984; ers. In the latter experiments, several re- Camazine, 1986; Rosenkranz et al, 1990). moved mites were found injured and had The consequence of this extremely low evidently been killed by the mellifera work- rate of reproduction is evident and not ers. We assume that cerana bees treat re- comparable to some seasonal variation in moved mites in the same manner. reproductive success, as reported for Var- roa populations in Europe (Blum, 1989; Ot- ten and Fuchs, 1990). The reasons for Varroatosis resistance such reproductive limitations still remain and mite reproduction unknown. Meanwhile, the various data available on host-parasite relationships between eastern as well as western honey The resistance mechanisms to varroatosis bees and Varroa jacobsoni point to a com- related to reproduction known up to now in plex of factors which are responsible for the original as well as the secondary host any tolerance towards of bees include parasitization by species honey obviously this mite. In particular, any inhibition of its various factors. In cerana it has been Apis reproduction (Rosenkranz, 1990a) plays a observed that adult workers re- rapidly decisive role in the population dynamics of move mites and ectoparasitic by grooming the parasite. This important aspect has to hence the invasion of brood cells prevent be considered more distinctly in breeding et al, however, these Varroa (Peng 1987); programs (Büchler, 1989) designed to se- females had also been collected from Apis lect strains of European honey bees toler- mellifera bees and this possibly explains ant to varroatosis. why they were readily attacked. An ex- tremely short duration of the post-capping Résumé — Reproduction de Varroa ja- phase of worker brood was determined in cobsoni dans des colonies d’Apis cera- Apis mellifera capensis (Moritz and Hänel, na indica en conditions naturelles et en 1984; Moritz and Mautz, 1990) and less conditions artificielles. Dans 10 colonies pronounced in other African (Moritz, 1985) d’Apis cerana indica à Allahabad (Inde), on compared to European races (Le Conte a contrôlé le parasitisme naturel du cou- and Cornuet, 1989; Büchler and Drescher, vain par Varroa jacobsoni en inspectant 2 1990; Schousboe, 1990). As a conse- fois par mois 100 cellules de couvain oper- quence, fewer female Varroa nymphs culé d’ouvrières, et 100 de mâles lorsqu’il y reach the adult stage. Attractivity of Apis en avait. Au printemps il n’y avait presque mellifera worker larvae to invading Varroa pas d’acariens sur le couvain d’ouvrières; females was found to be different accord- pendant la saison des pluies par contre et ing to the origin of the brood (Büchler, dans certaines colonies, plus de 5% des 1990). As confirmed by our studies, the dif- cellules d’ouvrières renfermaient des var- ferential hygienic behavior of Apis cerana roas femelles. Pourtant celles-ci ne se re- workers results in rather more mites re- produisaient pas. Sur le couvain de mâles, au contraire, tous les acariens étaient ferti- couvain d’ouvrières en termes de facteurs les. Le taux d’infestation du couvain de de résistance. Elle existe également, dans mâles de janvier à avril 1988 et 1989 a for- une moindre mesure, dans les colonies d’A tement varié d’une colonie à l’autre et mellifera africanisées tolérantes à la var- d’une année à l’autre et atteint 60% dans roatose. Si, dans nos expériences, 1/4 des certaines colonies (tableau I), la moyenne cellules d’ouvrières infestées artificielle- étant de 34% (fig 1). En conséquence ment n’a pas été nettoyé, cela peut être dû c’est le printemps, de janvier à avril à Alla- au fait que des varroas femelles ont été habad, qui a été choisi pour les essais. En prélevés et utilisés au sein de la même co- transférant les acariens des cellules ré- lonie d’A c indica. Par contre dans les ex- cemment operculées de mâles dans des périences réalisées par Rath et Drescher cellules récemment operculées d’ouvriè- (1990), les acariens, prélevés dans des co- res, on a voulu tester si les femelles de lonies d’A mellifera, ont été reconnus à Varroa réellement reproductrices réussis- l’odeur par les abeilles A c indica et donc saient à pondre après le transfert. éliminés presque totalement. Les facteurs de résistance connus liés à la Au cours de 2 périodes, on a ainsi reproduction des varroas prouvent que tout un ensem- transféré plus de 400 varroas femelles. ble de facteurs est responsable de la tolé- Lors d’essais préliminaires on avait obser- rance à la varroatose. Les causes n’ont été vé que des varroas, rassemblés pour une étudiées. Nous infestation artificielle dans d’autres colo- qu’insuffisamment pensons un rôle décisif revient nies, avaient été éliminés sur-le-champ que, parmi celles-ci, à l’infertilité des varroas femelles liée à après transfert dans les cellules opercu- l’hôte. Une plus grande importance doit lées d’ouvrières. Cela se produisait en par- être accordée à ce facteur dans les futurs ticulier lorsque les acariens provenaient de programmes destinés à sélectionner des li- colonies d’Apis mellifera. Aussi, dans tou- gnées d’A mellifera résistantes à Varroa. tes les autres expériences, n’avons nous transféré des varroas femelles qu’au sein Apis cerana / Varroa jacobsoni / repro- d’une même colonie d’A c indica. Huit à dix duction / infertilité / résistance à la var- les acariens avaient jours plus tard, dispa- roatose ru de 75% des cellules d’ouvrières infes- tées artificiellement. Les cellules étaient en et renfer- pourtant majorité operculées Zusammenfassung — Fortpflanzung maient une nymphe d’abeille. De toute évi- von Varroa jacobsoni in Völkern von dence, les abeilles les avaient réopercu- Apis cerana indica unter natürlichen lées. Nous n’avons malheureusement pas und experimentellen Bedingungen. Bei pu observer si les varroas étaient éliminés, zehn Völkern von Apis cerana indica et les abeilles ou si cel- peut-être tués, par wurde in Allahabad, Indien, der natürliche les-ci ne contrôlaient et n’ouvraient les que Befall der Brut durch Varroa jacobsoni kon- cellules nous et laissaient manipulées par trolliert, indem zweimal pro Monat je 100 les varroas s’en Sur les 100 var- échapper. verdeckelte Arbeiterinnen- und, falls vor- roas retrouvés, 12% seulement, soit 3% handen, Drohnenzellen untersucht du nombre total de femelles transplantées, wurden. Während des Frühjahrs wurden in avaient Aucune pondu (tableau II). nym- der Arbeiterinnenbrut fast keine Milben ge- phe éclose n’a été trouvée. funden, während der sommerlichen Re- Nous discutons de la signification de genzeit enthielten dagegen in einigen Völ- cette infertilité des varroas femelles sur le kern über 5% der Arbeiterinnenzellen Varroa-Weibchen. Diese pflanzten sich setzten Varroa-Weibchen entspricht, Eier jedoch nicht fort. In Drohnenbrut waren da- abgelegt (Tabelle II). Geschlüpfte Nym- gegen alle Milben fertil. Der Infektionsgrad phen fanden wir nicht. Die Bedeutung der Drohnenbrut lag in den Monaten dieser Unfruchtbarkeit von Varroa- Januar-April 1988 und 1989 in einzelnen Weibchen in Arbeiterinnenbrut als Resis- Völkern bei bis zu 60% (Tabelle I), wobei tenzfaktor wird diskutiert. Sie ist in schwä- von Volk zu Volk und in den beiden Jahren cherem Maße auch bei den ebenfalls Var- erhebliche Schwankungen festgestellt roatose-toleranten afrikanisierten Apis mel- wurden. Die Mittelwerte des Drohnenbrut- lifera-Völkern in Brasilien ausgeprägt. Daß befalls erreichten 34% (Abb 1). Das zeitige in unseren Versuchen rund 1/4 der künst- Frühjahr, in Allahabad Januar-April, wurde lich infizierten Arbeiterinnen-Brutzellen daher für Versuche gewählt, bei denen nicht ausgeräumt wurde, könnte darauf be- durch Umsetzen von Milben zwischen ver- ruhen, daß hierfür erstmals nur innerhalb deckelten Drohnen- und Arbeiterinnenzel- derselben Apis cerana-Völker gesammelte len geprüft werden sollte, ob reproduk- Varroa-Weibchen verwendet wurden. Hin- tionsaktive Varroa-Weibchen zur Eiablage gegen sind bei ähnlichen Experimenten gelangen, wenn sie in Arbeiterinnenbrut anderer Autoren (Rath und Drescher, gebracht werden. Innerhalb von zwei Ver- 1990) durchweg aus Apis mellifera-Völkern suchsperioden wurden über 400 Varroa- gewonnene Milben eingesetzt worden, die Weibchen aus kürzlich verdeckelten Droh- möglicherweise von den Apis cerana- nenzellen in ebensolche Arbeiterinnenzel- Bienen am Geruch erkannt und deswegen len umgesetzt. In Vorversuchen hatten wir fast gänzlich eliminiert wurden. Die bis beobachtet, daß Milben, die für eine künst- jetzt in Zusammenhang mit der Milben- liche Infektion in anderen Völkern gesam- Fortpflanzung bekannt gewordenen Resi- melt worden waren, nach Einsetzen in ver- stenzfaktoren weisen darauf hin, daß eine deckelte Arbeiterinnenbrut alsbald ausge- Varroatose-Toleranz offensichtlich durch räumt wurden. Dies erfolgte insbesondere einen Komplex verschiedener Faktoren be- dann, wenn die Milben aus Apis mellifera- dingt ist. Deren Ursachengefüge ist erst Völkern stammten. In allen weiteren Versu- unzureichend erforscht worden. Wir chen haben wir daher die Varroa- meinen, daß dabei einer wirtsbedingten Weibchen stets innerhalb desselben Apis Unfruchtbarkeit der Milbenweibchen eine cerana indica-Volkes umgesetzt. Acht bis entscheidende Bedeutung zukommt. In zehn Tage später waren aus ca 300 der künftigen Arbeitsprogrammen für eine Aus- künstlich infizierten Arbeiterinnenzellen lese Varroatose-resistenter Linien von Apis trotzdem die Milben verschwunden. Die mellifera sollte diesem Faktor größere Be- Mehrzahl dieser Zellen wurde jedoch ver- deutung beigemessen werden. deckelt vorgefunden und enthielt eine Bie- nenpuppe. Offensichtlich hatten die Bienen Apis cerana / Varroa jacobsoni / Repro- die Zellen wieder verschlossen. Leider duktion / Infertilität / Varroatose- konnten wir nicht beobachten, ob die Resistenz Milben gezielt ausgeräumt und vielleicht von den Bienen getötet wurden, oder ob diese nur die von uns manipulierten Zellen REFERENCES kontrollierten, öffneten und dabei eventuell die Milben entweichen ließen. Von den Abbas ND, Engels W (1989) Rearing of Varroa über 100 wiedergefundenen Milben hatten in artificial cells on drones. In: Present Status nur 12%, was 3% der insgesamt umge- of Varroatosis in Europe and Progress in the Varroa Mite Control (Cavalloro R, ed) EC Varroa jacobsoni (Mesostigmata: Acari) by a Publ, Luxembourg, 223-228 host’s hormone: juvenile hormone III. J Insect Blum R (1989) Reprodukion der Varroa-Milbe Physiol 32, 791-798 bei unterschiedlicher Protein-Versorgung der Issa MRC, Gonçalves LS (1984) Study of prefer- Bienenvölker. Apidologie 20, 509-512 ence of the acarid Varroa jacobsoni for Boecking O, Drescher W (1991) Response of drones of Africanized honeybees. 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