The effects of climate and race on jacobsoni Oud infestations in Brazil G Moretto, Ls Gonçalves, D de Jong, Mz Bichuette

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G Moretto, Ls Gonçalves, D de Jong, Mz Bichuette. The effects of climate and bee race on Oud infestations in Brazil. Apidologie, Springer Verlag, 1991, 22 (3), pp.197-203. ￿hal- 00890907￿

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The effects of climate and bee race on Varroa jacobsoni Oud infestations in Brazil

G Moretto LS Gonçalves D De Jong MZ Bichuette

1 University of São Paulo, Faculty of Medicine, Genetics Department, Riberão Preto-SP; 2 University of São Paulo, Faculty of Philosophy, Sciences and Letters, Biology Department, Riberão Preto-SP; 3 University of São Paulo, Faculty of Philosophy, Sciences and Letters, Department of Geology Ribeirão Preto Campus, 14 049 Ribeirão Preto, SP, Brazil

(Received 28 June 1990; accepted 25 February 1991)

Summary — Varroa jacobsoni infestation rates on adult Africanized and Italian/Africanized hybrid honey were measured in 3 different climatic regions of Brazil : Ribeirão Preto, Rio do Sul and São Joaquim (mean temperatures 21, 18 and 13 °C, respectively), over a 2-yr period. The mean in- festation rates were 3.5, 5.11 and 11.37 per 100 bees in the 3 regions respectively, demon- strating that climate type has a strong influence and that infestation rates are higher in the cooler re- gions. The type of bee also had an important effect, as the Italian hybrids were significantly more infested than the Africanized bees (7.53 and 5.78 mites per 100 bees, respectively). Varroa jacobsoni / infestation rate / Africanized honeybee / climate

INTRODUCTION The impact of a Varroa infestation de- pends on the degree of infestation in the bee colony. A low infestation apparently while the Originally, ectoparasitic causes little damage, while a high infesta- Varroa jacobsoni Oud (, Varroidae) tion eventually leads to colony death. was confined to the Asian , In Apis mellifera colonies the popula- , was not serious- tion dynamics of Varroa jacobsoni differs affected due to the low of infes- ly degree in the various regions of the world. For ex- tation generally found on its original host ample, in west Germany, the mite popula- et De et (Koeniger al, 1981; Jong al, tion increases 10-fold from spring to sum- after the mite came into 1982). However, mer (Schulz et al, 1983), while in other contact with it caused Apis mellifera, countries, such as Brazil and Uruguay, much more serious problems, was spread the situation is much different, as the mite to many other parts of the world, and re- has been established for more than 10 yr sulted in the death of hundreds of thou- and the population remains at a low level sands of colonies of the latter (De (De Jong et al, 1984; Ruttner et al, 1984; Jong et al, 1982). Gonçalves, 1987).

* Correspondence and reprints One factor that directly affects the final Brazil and high terminal infestations in the population of Varroa in the bee colonies is Buenos Aires province of Argentina (De the percentage of female mites which re- Jong et al, 1984). We assume that the ge- produce when they enter worker brood netic composition of the V jacobsoni popu- cells. This percentage is considerably low- lations is the same, since they were from er in tropical and subtropical Latin America the same introduction. However, it is diffi- when compared with temperate areas of cult to separate the effects of climate and Europe and the Middle East (Ritter and De bee race, as in Brazil the bees are African- Jong, 1984). ized and in that region of Argentina they Bee race also seems to be an important are European (Kerr et al, 1982). factor for determining the success of the The objective of our research was to de- mites as significantly fewer female Varroa termine the relative importance of climate that entered worker brood cells achieved and honey bee race for Varroa infesta- successful reproduction in Africanized bee tions. colonies than in European (Italian or Carni- olan) colonies, even when they were kept in the same apiary in Brazil (Camazine, MATERIALS AND METHODS 1986; Rosenkranz, 1986). The bee, mellifera cape Apis capensis, This experiment was conducted in 3 distinct cli- has a very much shortened sealed-cell matic regions. The 3 regions have been classi- stage, 2.4 d less in the workers when com- fied according to Köppen (1948) by Andrade pared with A m carnica. The reproductive (1964): Ribeirão Preto, São Paulo state, 620 m potential of the mites is considerably lower altitude, 21 °11’25" south latitude, with an aver- mean of a humid in the former, as most mite nymphs are age temperature 21 °C, tropi- cal well defined a hot not able to reach the adult (Moritz climate, seasonally by stage summer > 23 °C and > and the rainy (mean temperature Hänel, 1984). However, though 250 mm of rain in the hottest month) and dry sealed-cell stage of worker Africanized and mild winter season (mean minimum temper- bees is ≈ 20 h shorter than that of Euro- atures ≈ 18 °C and < 30 mm precipitation in the pean bees, the number of mite offspring coldest month); Rio do Sul, Santa Catarina produced per female mite (including only state, 354 m altitude, 28°17’55" south latitude, with an mean of 18 °C, a those that successfully reproduce) is near- average temperature humid mesothermic climate without a distinct the same ly (Rosenkranz, 1986). dry period and the mean temperature of the hot- Pure A m carnica colonies kept in Ri- test month > 22 °C, climate typical of southern beirão Preto, Brazil, had significantly high- Brazil; and São Joaquim, Santa Catarina state, 1 360 m altitude, 28°17’19" south latitude, with er infestations than "wild type" Africanized an average mean temperature of 13 °C, a humid bee colonies in the same apiary, though mesothermic climate, with no distinct dry period were also much less infested than they and the mean temperature of the hottest month sister Carniolan colonies kept in Germany not reaching 22 °C; climate typical of the higher (Engels et al, 1986). mountain regions (1 200-1 600 m). In addition, mean were obtained from Differences in the infestation rate of V monthly temperatures government monitoring stations. jacobsoni could be influenced by bee race, Each apiary was set up with bees of 2 racial climate, origin of the mite or some combi- Africanized bee colonies were headed by nation of these factors. In South types. America, queens reared from descendants of natural where V jacobsoni was apparently intro- swarm queens captured in the region of Ri- duced from Japan in = 1970 (De Jong et beirão Preto. The wild honey bees in this part of al, 1982), we find low stable infestations in Brazil have predominantly African (Apis mellife- ra adansonii, now called Apis mellifera scutella- appear), measured in number of mites per ta) characteristics (Lobo et al, 1989). 100 bees for the São Joaquim, Rio do Sul Italian hybrid colonies were headed by and Ribeirão Preto apiaries were 17.10, queens reared from Italian queen mothers im- 1.10 and 1.86, respectively, for the hives from the USA and and from artifi- ported Italy, requeened with Africanized queens, and cially inseminated maintained at the ex- queens 20.10, 1.23 and 1.28 for those perimental apiary of the Genetics Department at requeened the University of São Paulo in Ribeirão Preto. All with Italian queens. of the virgin queens were open-mated with wild Subsequently after the bees were all type Africanized drones in the Ribeirão Preto substituted, the infestation rates calculated Thus there was one of apiary. group consisting the course of the for the 3 lo- Africanized bee colonies and another of Italian/ during study Africanized hybrid bee colonies. cations showed no significant interaction effects between race and climate (F = The apiaries were installed in March 1986. Twelve standard single-storey Langstroth hives 0.62) though there was a significant race populated with bees of each region were select- effect (F = 5.23; P < 0.05), as Italian hy- ed and numbered for each of the 3 experimental brids were more susceptible than the Afri- apiaries. Half of the colonies, selected random- canized bees (7.53 and 5.78 mites per 100 ly, were requeened with Africanized queens and bees, respectively). the other half with open-mated Italian queens in April and May of 1986. During the course of the Climate type had a highly significant in- study, whenever any queen was lost, it was re- fluence on the mite infestations (F = 28.6; placed with another of the same type, also P < 0.001) and apparently was more im- reared and mated in Ribeirão Preto. portant than race. A multiple comparison Preliminary infestation data were collected in analysis, comparing the locations 2 by 2, March and April, 1986. Adult bee infestations demonstrated that the bees in São Joa- were estimated using a methodology developed quim (11.37 mites per 100 bees) were sig- by Stort et al (1981). Samples of 200-500 adult more infested than those in Rio bees from each colony were brushed from 2 or nificantly do Sul mites 100 and Ri- 3 brood combs into beakers partially filled with = (5.11 per bees) 250 ml of weak detergent solution. These were agitated and then strained to separate and count the bees and mites. By June 1986, all the bees in the colonies were progeny of the intro- duced queens. The colonies were then sampled once a month from June 1986 to February 1988. The total infestation rate was analyzed with a fixed model analysis of variance with 2 classifi- cation criteria and when necessary, a Tukey’s multiple comparison test was performed. The data were transformed (y = log (p/(1-p)) to stabi- lize the variance. During the 2-yr course of the experiment, several colonies were lost. The analyses were therefore restricted to 4 colonies of each racial type for each of the experimental apiaries.

RESULTS

The initial infestation rates (before the new workers of the introduced queens began to beirão Preto (3.5 mites per 100 bees), and infestation rate was already high (> 10 that the bees in Rio do Sul were more in- mites per 100 bees). The mites were prob- fested than those in Ribeirão Preto (figs 1, ably introduced through migratory bee- 2). keeping practices (De Jong, unpublished No information was availa- Mean monthly temperatures are given data). previous ble in Rio do in figure 3. In general terms we could ob- concerning infestations Sul; it is ≈ 150 km São Joa- serve that the greater the annual mean however, only from temperature, the lower the mean infesta- quim. Unlike São Joaquim, which is an im- tion rate. portant beekeeping region because of the seasonally abundant wildflowers and the widespread use of bees for apple pollina- DISCUSSION AND CONCLUSION tion, there is not much movement of bees into or out of Rio do Sul. So we presume Varroa jacobsoni was apparently intro- that the infestation there was introduced a duced into Brazil about 1971 or 1972, year or two later. through infested bees transported from It is apparent that climate type has a Paraguay to São Paulo State (De Jong significant impact on Varroa populations. and Gonçalves, 1981). Now, more than 10 The infestation rates we observed in São yr after the mites spread throughout the Joaquim, one of the few places in Brazil state, we find that the infestation rates where snow falls on occasion, were much have stabilized at ≈ 3 mites per 100 bees higher than those we have encountered in (Gonçalves, 1987). other areas. Even though the mites did not Varroa probably arrived in the São Joa- completely destroy the colonies as they do quim area about 1983 or 1984. An inspec- in Europe (De Jong et al, 1982), the infes- tion of 8 apiaries, belonging to different tations in some colonies in São Joaquim beekeepers, made there in 1984 showed were high enough to retard their develop- only one apiary to be infested, though the ment and compromise their production. During much of the study, the infesta- seasons. Possibly physiological changes tion rates in hybrid and Africanized colo- in the bees, mediated by climate, have nies were little different in both Rio do Sul some effect on Varroa reproduction and and São Joaquim, except in the late fall survival. De Jong (1981) found that when and winter (April-August) in São Joaquim, the bee colony produces emergency when they were much higher in the Euro- queen cells, the number of mites entering pean/Africanized hybrids (figs 1, 2). In Ri- worker brood cells increases ≈ two and a beirão Preto the fact that infestation levels half times, which demonstrates that the were higher in the hybrid bees was more mites do react to changes in colony condi- consistently evident. tions. In Ribeirão Preto, the most tropical of The Africanized bees were more resist- the 3 regions, there was little monthly vari- ant to Varroa infestations than the hybrid ation in the infestation rates. The in- Italian bees, a result also confirmed by creased infestation rates during fall and Mendoza et al (1987) in Paraguay, though winter were most evident in the coolest re- the difference was not as strong as that gion (São Joaquim), and somewhat less found between the different climatic re- so in the intermediate climate region (Rio gions we studied. do Sul, figs 1, 2). Some of this difference could be attributed to the reduction in brood and adult bee population during the ACKNOWLEDGMENTS colder months. As the number of brood cells available diminished more of the We thank R Pries of the Instituto de Apicultura mites in the colony would be on the adult do Estado de Santa Catarina (IASC) for donat- bees, and as the adult bee population de- ing the bees used in the São Joaquim apiary, clined, the mites would be distributed and PB Primo, director of the Centro de Treina- among fewer bees, increasing the appar- mentos de São Joaquim (CETREJO) for provid- an site and for anal- ent infestation, measured in mites per bee. ing apiary laboratory space yses. We also thank JJ dos Santos of the Interestingly, unlike Varroa infestations Department of Genetics for assistance in collect- in Europe which increase rapidly over a ing data, maintaining colonies and producing period of 1-4 yr, by which time critical lev- queens in the Ribeirão Preto apiary. G de Sordi, of the Institute of director of the São els are reached (De Jong et al, 1982), the Agronomy, Paulo State Farm in Ribeirão Pre- infestations within the 3 experimental api- Experimental to, metereological data for the Ribeirão aries did not increase overall the 2 provided during Preto area and P de Alcantara Ribeiro of EM- yr that they were monitored. PASC in São Joaquim and D Gandin of EM- the By using queens all issued from the PASC in Ituporanga provided meterological data for São and Rio do Sul, same lines and reared and mated in the Joaquim respec- tively. This work was funded by the Financiado- same location, we showed that the climatic ra de Estudos e Projetos (FINEP), with some a of effects were not merely consequence additional assistance from a CNPq grant to LS the variation in susceptibility of the differ- Gonçalves and from USDA-OICD and NSF ent types of bees adapted to each climate (DAR 7920922) grants to RA Morse. region. However, it is not clear how climat- ic differences would affect the Varroa mites when one considers the fact that the Résumé — Influence du climat et de la mite reproduction is accomplished within race des abeilles sur les infestations the brood cells, which the bees maintain at par Varroa jacobsoni Oud au Brésil. On a constant temperature (= 34 °C) during all a pu montrer que le climat et la race des abeilles étaient des facteurs importants du différence ne soit pas aussi remarquable niveau d’infestation des colonies d’abeilles que celle due au climat. (Apis mellifera L) par Varroa jacobsoni Oud (Acari, Varroidae) au Brésil. Varroa jacobsoni / taux de parasitisme / climat / abeille africanisée Trois ruchers comportant chacun 6 co- lonies d’abeilles africanisées et 6 colonies italiennes/africanisées, ont été d’hybrides Einfluß von Klima installés à Ribeirão Preto de São Zusammenfassung — 1) (État und Bienenrasse auf den Varroabefall Paulo), région tropicale, température an- in Brasilien. Es konnte werden, nuelle de 21 à Rio do Sul gezeigt moyenne °C; 2) daß sowohl der wie die Bienen- de Santa climat humide Klimatyp (État Catarina), rasse in Brasilien Faktoren für modérément annuelle wichtige chaud, température den der Bienenvölker mit de à São Befallsgrad moyenne 18 °C; 3) Joaquim (état Varroa sind. de Santa Catarina), climat humide modé- rément chaud, température annuelle Drei Bienenstände, jeder mit 6 Völkern afrikanischer und mit 6 moyenne de 13 °C, l’un des rares endroits Abstammung Hy- bridvölkern Italiener x Afrikanisierte Biene, du Brésil où il neige un peu en hiver. Tou- wurden 1986 an Orten errichtet: tes les reines ont été élevées et se sont folgenden accouplées naturellement dans le rucher 1. - Ribeiräo Preto, Staat Säo Paulo, ein Gebiet mit einer mittleren Jah- de Ribeirão Preto de sorte que les mêmes tropisches restemperatur von 21 °C; 2. - Rio do Sul, lignées ont été utilisées dans les 3 en- Staat Santa mit einem droits. Un contrôle des colonies a été fait Catarina, feuchten, warmes Klima, mittlere Jahrestem- mois, de 1986 à février 1988 mäßig chaque juin 3. - Säo Staat déterminer le taux de des peratur 18 °C; Joaquim, pour parasitisme Santa mit feuch- abeilles adultes. Des échantillons de 200- Catarina, mäßig warmem, ten Klima, mittlere 13 °C 500 abeilles ont été sur les ca- Jahrestemperatur prélevés - einer der wenigen Orte in Brasilien, an dres de couvain et dans un réci- placés dem im Winter etwas Schnee fällt. Alle Kö- pient avec un détergent léger. Les abeilles niginnen wurden am Bienenstand von ont été secouées et au crible passées Ribeiräo Preto aufgezogen und natürlich pour les séparer des acariens et dénom- begattet, so daß an allen drei Standorten brer ceux-ci. Certaines colonies ont été dieselben Linien benutzt wurden. Die perdues au cours de l’expérience, les ana- Völker wurden in monatlichen Abständen ont donc sur 4 colonies de cha- lyses porté von Juni 1986 bis Februar 1988 kontrol- race dans rucher 24 colo- que chaque (soit liert, um den Befallsgrad der erwachsenen nies au total). Bienen zu bestimmen. Dazu wurden von Les taux moyens de parasitisme ont été Brutwaben Proben von 200-500 Bienen in de 11,37, 5,11 et 3,5 acariens pour 100 einen Becher mit einer schwachen Wasch- abeilles à São Joaquim, Rio do Sul et Ri- mittellösung gekehrt. Die Bienen wurden beirão Preto respectivement. Ceci prouve gerührt und gesiebt, um Bienen und que le climat exerce une forte influence et Milben getrennt zählen zu können. Einige que les régions plus froides sont les plus Völker gingen während des Versuches ver- parasitées. La race joue aussi un rôle : les loren, deshalb beruhen die Analysen nur hybrides italiennes ont été significative- auf vier Völkern jeder Rasse auf jedem der ment plus parasitées que les abeilles afri- drei Standorte (24 Völker insgesamt). canisées (7,53 et 5,78 acariens pour 100 Die mittlere Befallsrate betrug in Sao abeilles, respectivement), bien que cette Joaquim, Rio do Sul und Ribeiräo Preto 11.37, 5.11 und 3.5 Milbe je 100 Bienen; of the Africanized bee in South America. Am das zeigt einen starken Einfluß des Klima- Bee J 122, 196-198 typs, wobei die Befallsraten in den kühle- Koeniger N, Koeniger G, Wijayagunasekara ren Regionen höher sind. Es zeigte sich NHP (1981) Beobachtungen über die Anpas- aber auch ein deutlicher Einfluß der Ab- sung von Varroa jacobsoni an ihren natürlichen Wirt cerana in Sri Lanka. stammung der Bienen: Die Italiener- Apis Ap- idologie 12, 37-40 Hybriden waren signifikant stärker befallen als die Afrikanisierten Bienen Köppen LW (1948) Climatologia. Com un Estu- (7.53 gegen dio de los Climas de la Tierra. Fondo de Cul- 5.78 Milben 100 Bienen. Dieser Unter- je tura Econômica, Panuco 63, Mexico, DF schied war jedoch nicht so eindrucksvoll Lobo JA, Del Lama MA, Mestriner MA wie der zwischen den (1989) Klimagebieten. Population differentiation and racial admix- ture in the Africanized honey bee (Apis mellif- Varroa jacobsoni / Einfluß des Klimas / era L). 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