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NOTES sampled worker bees of 13 colonies. Using a molecular technique that distinguishes European from Africanized bees we found that nine sampled colonies were Africanized and four were European by maternal descent. The lack of a complete genetic sweep by Africanized bees contrasts greatly with the population in Puerto Rico and populations studied in the mainland. Even though the presence of European bees on the island may be due to input from the apicultural sector, it is highly likely that other factors, such as island climate, the lack of a continuous influx of Africanized bees, and the absence of Varroa mites, a common pest of European bees has allowed their survival. KEYWORDS.—Africanized honey bees, Apis, West Indies, invasive species, Varroa
Caribbean Journal of Science, Vol. 44, No. 2, 264-266, 2008 Copyright 2008 College of Arts and Sciences University of Puerto Rico, Mayagu¨ ez
Coexistence of Feral Africanized and European Honey Bees (Hymenoptera: Apoidea: Apidae) on St. Croix Island BERT RIVERA-MARCHAND1,2, JOZEF KEULARTS3, DEVRIM OSKAY4 AND TUGRUL GIRAY4 1Corresponding Author (
[email protected]), 2 Inter American University of Puerto Rico, Bayamón Campus, 500 John Will Harris Rd., Bayamón, PR 00957, 3Cooperative Extension Service University of the Virgin Islands, St. Croix, VI 00850, 4University of Puerto RicoRío Piedras Campus, Department of Biology, PO Box 23360 San Juan, PR 00931 ABSTRACT.—The first evaluation of the feral population of honey bees on the island of St. Croix, US Virgin Islands is performed. Since Africanized bees had been reported in 1994, we expected that, as in the neighboring island of Puerto Rico, the feral population of St. Croix would be strongly Africanized. We
Honey bees (Apis mellifera) were introduced to the Western Hemisphere during colonial times (Sheppard 1989). Among the different bee subspecies or races that historically have been preferred are those of European origin. European honey bees are known to produce greater amounts of honey and be relatively docile. However, these bees tend to be poorly adapted to the Tropics. To cope with this problem, tropical African bees (Apis mellifera scutellata) were brought to Brazil in 1956 (Kerr 1967). The aim was to produce a hybrid between the African bee and European races that would be as adapted to the tropics as the African bees, yet produce honey and be as manageable as European bees. However, some swarms escaped and rapidly hybridized with feral European bees producing the Africanized bee. Africanized bees have retained tropical adaptations including high defensive behavior and parasite resistance throughout their range in continental America (Schneider et al. 2004). Africanized honey bees are among the most important invasive species in the Western Hemisphere. These bees have invaded most of continental America, their distribution however, is limited mainly by areas with cold weather. In 1994 the Africanized bees invaded the Caribbean. The first report of these bees in the Caribbean was in Puerto Rico (Cox 1994). However, within the same year they were reported on the Island of St. Croix of the US Virgin Islands (Stanford 1996) the second of three
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known Caribbean islands known to have Africanized bees (the third is Hispaniola). Although their presence has been confirmed by the US Department of Agriculture, a thorough study of the feral honey bee population had not been performed. The purpose of this study was to provide an evaluation of the extent of Africanization on the Caribbean island of St. Croix. We hypothesized that, as with the island of Puerto Rico (Rivera-Marchand 2006), the feral population of honey bees of St. Croix is Africanized by maternal descent. To evaluate the levels of Africanization we sampled 13 feral colonies throughout the 207 km2 island in April, 2004. We captured ten worker bees per colony, immediately placed them in 95% ethanol and stored them at −20°C. To assure that the sampled bees were from the studied colony, we only took foragers returning to the colony. Moreover, to avoid the possibility of sampling drifting foragers we sampled hives that were at least 1km apart. We extracted DNA from the thorax of one of the workers from each colony using the Qiagen® DNA Easy Extraction Kit, following the animal tissue protocol. To determine Africanization by maternal descent we followed the restriction fragment length polymorphism (RFLP) protocol developed by Nielsen et al. (2000). The method distinguishes Africanized bees from bees having Western European, Eastern European and Egyptian origin through their mitochondrial DNA. We amplified a region of the rDNA of approximately 964bp. The PCR product was then digested with the restriction enzyme EcoRI. This enzyme digests the PCR product of the Eastern European bees into two bands of 480 and 484bp. The samples were visualized in a 1% agarose gel stained with ethidium bromide. Of the sampled feral colonies of St. Croix nine were Africanized while four were Eastern European by maternal descent (see Fig.1 for distribution according to race). Even though our sample size is reduced it clearly shows that, although the feral population of bees is predominantly Africanized, there are still feral colonies that are European by maternal descent on the island. These results contrast with results ob-
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FIG. 1. Distribution of sampled feral honey bee colonies by race, as determined by a mtDNA assay, on the island of St. Croix. The letter “A” represents samples that are Africanized, while the letter “E” represents samples that are European.
tained from studies in the mainland as well as on the island of Puerto Rico. In Texas, USA there was a total replacement of European bees by Africanized bees within five years of their arrival (Pinto et al. 2005). Whitfield et al. (2007) report a near replacement of European alleles by Africanized alleles, throughout the New World. In Puerto Rico, Rivera-Marchand (2006) also found similar results, where all sampled colonies were Africanized by maternal descent. The coexistence of these races in St. Croix may be due to an input from the small beekeeping sector, a lack of influx of Africanized bees on the island or perhaps the absence of honey bee pests, particularly Varroa mites. There are no known large commercial apiaries on the island (they are mainly hobbyists), therefore it is possible that the input from beekeepers may be a minor factor allowing the presence of European bees. Since St. Croix is an island, its isolation may have caused a lack of influx of Africanized bees, a process that has allowed the complete replacement of European bees in places like Yucatan, Mexico (Clarke et al. 2002). However, if this were the case it would contrast greatly with the neighboring island of Puerto Rico where under similar isolation and with a larger beekeeping sector, Africanized bees have replaced European bees (Rivera-Marchand 2006). Varroa mites have not been reported on the island and they were not found in any of our samples. This absence of Varroa mites may be an important factor explaining the coexistence of European and Africanized bees.
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Varroa mites are known to decimate European bees (Martin et al. 1998). Africanized bees however, are resistant to these parasites (Rivera-Marchand 2006). The impact of these parasites on the feral European population may have facilitated the spread of Africanized honey bees in places such as the island of Puerto Rico and southern United States. Besides the absence of Varroa mites on the island environmental factors related to the island may also play an important role in the coexistence of European and Africanized bees. Although Africanized bees are known to have a competitive advantage over European bees in the Tropics (Breed et al. 2004) this may be different on islands. Islands have limited space and resources. To survive, honey bees on islands must store honey for times where there are few flowers available such as prolonged droughts or after a hurricane. In absence of Varroa, honey hoarding European bees may have been able to survive on St. Croix longer than in Puerto Rico in the presence of Africanized bees. Models of Africanization and spread of bee populations should take in to consideration factors such as resources and diseases in addition to temperature, and introduction time. The results of this study imply the importance of understanding the role of biotic (e.g., parasites) and abiotic (e.g., climate) factors that affect invading species, particularly on islands. Acknowledgments.—We thank A. Rodríguez-Durán for reviewing an earlier version of the manuscript. We thank the Center for Research Excellence in Science and Technology Program-Center for Applied Tropical Ecology and Conservation-National Science Foundation for providing the necessary funding for this project. LITERATURE CITED Breed M. D., E. Guzmán-Novoa, and G. J. Hunt. 2004. Defensive behavior of honey bees: Organization, genetics, and comparisons with other bees. Ann. Rev. Entomol. 49: 271-298. Clarke K. E., T. E. Rinderer, P. Franck, J. G. QuezadaEuán, and B. Oldroyd. 2002. The Africanization of honeybees (Apis mellifera L.) of the Yucatan: A
study of massive hybridization event across time. Evolution 56(7): 1462-1474. Cox, B. 1994. AHB in Puerto Rico. Amer. Bee Journal 134(10): 668. Kerr, W. E. 1967. The history of the introduction of African bees to Brazil. South Afr. Bee J. 39: 3-5. Martin, S. J., A. Hogarth, J. Van Breda, and J. Perett. 1998. A scientific note on Varroa jacobsoni Oudemans and the collapse of Apis mellifera L. colonies in the United Kingdom. Apidologie 29: 369-370. Nielsen, D. I., P. R. Ebert, R. E. Page Jr., G. J. Hunt, and E.Guzmán-Novoa. 2000. Improved polymerase chain reaction-based mitochondrial genotype assay for the identification of the Africanized honey bee (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 93(1): 1-6. Pinto, M. A., W. L. Rubnik, J. C. Patton, R. N. Coulson, and J. S. Johnston. 2005. Replacement of Feral European Honeybees (Apis mellifera L.) by an African Hybrid Swarm. Genetics 170: 1653-1665. Rivera-Marchand, B. 2006. Africanized Bees in Puerto Rico. PhD Thesis. University of Puerto Rico, Río Piedras. 100pp. Sanford, M. T. 1996. What of the Africanized honey bee? APIS 14(9):1. Schneider, S. S., G. DeGrandi-Hoffman, and D. R. Smith. 2004. The African honey bee: factors contributing to a successful invasion. Ann. Rev. Entomol. 49: 351-376. Sheppard, W.S. 1989. A history of the introduction of honey bee races into the United States. American Bee Journal 129:617-619. Whitfield, C. W., S. K. Behura, S. H. Berlocher, A. G. Clark, J. S. Johnston, W. S. Sheppard, D. R. Smith, A. V. Suarez, D. Weaver, and N. D. Tsutsui. 2007. Thrice out of Africa: Ancient and recent expansions of the honey bee, Apis mellifera. Science 314: 642-645.
