Introducción de abejorros (Bombus) no nativos: causas, consecuencias ecológicas y perspectivas

  • Carolina L. Morales Laboratorio Ecotono, Universidad Nacional del Comahue, Bariloche, Río Negro, Argentina.
Palabras clave: cría comercial de abejorros, hibridación, desplazamiento competitivo, especies exóticas, invasiones biológicas, patógenos, polinización de cultivos

Resumen

La invasión de polinizadores no nativos puede afectar considerablemente a los polinizadores nativos y a las plantas, nativas e introducidas. En este trabajo analizo las causas de la introducción de abejorros (Bombus) polinizadores, los factores que favorecen su invasión y la distribución de las especies introducidas; reviso los estudios sobre sus impactos ecológicos; las limitaciones y de los principales vacíos de conocimiento. Existen cinco especies de abejorros establecidas fuera de sus áreas de distribución natural, producto de la liberación intencional y del comercio de colonias. Los abejorros introducidos son altamente polilécticos, pueden alcanzar altas abundancias en las áreas invadidas y, en algunos casos, dominar las comunidades antófilas. En general, adquieren recursos de manera más eficiente que las especies nativas y, a pesar de un sustancial solapamiento en el uso de flores, se excluyen mutuamente tanto espacial como temporalmente, lo que sugiere una potencial competencia con especies nativas, aún no documentada experimentalmente. La introducción de abejorros podría favorecer la introducción y transmisión de patógenos. Son polinizadores menos eficientes de algunas plantas nativas que sus congéneres nativos. En general, prefieren especies de plantas no nativas lo que contribuye sustancialmente a la polinización de importantes malezas, si bien su efecto sobre la capacidad de invasión de las mismas no ha sido evaluado. Algunas especies de abejorros no nativos pueden cruzarse con congéneres nativos en condiciones experimentales, si bien no se han documentado hibridaciones en la naturaleza. La evidencia del impacto de abejorros introducidos sobre ecosistemas nativos es escasa, fragmentada y preliminar. No obstante, sugiere que la aplicación del principio precautorio al momento de analizar la viabilidad de futuras introducciones sería altamente recomendable.

Citas

ABRAHAMOVICH, A; MC TELLERIA & NB DAIS. 2001. Bombus species and their associated flora in Argentina. Bee World, 82: 76–87.

AIZEN, MA & P FEINSINGER. 2003. Bees not to be? Responses of insect pollinator faunas and flower pollination to habitat fragmentation. Pp 112–119 in: G Bradshaw P Marquet & HA Mooney (eds.). How landscapes change: human disturbance and ecosystem disruptions in the Americas, Springer- Verlag, New York

ANDERSON, DL & JWH TRUEMAN. 2000. Varroa jacobsoni (Acari: Varroidae) is more than one species. Experimental and Applied Acarology, 24: 165-189.

ANDERSON, DL. 1997. Evaluation of quarantine risks associated with importations of the leafcutter bee (Megachile rotundata) to Australia from Canada. Report Commissioned by the Australian Quarantine Inspection Service. 45 pp.

ARRETZ, PV & RP MACFARLANE.1986. The introduction of Bombus ruderatus to Chile for red clover pollination. Bee World, 67: 15–22.

BALL, BV & MF ALLEN. 1988. The prevalence of pathogens in honey bee colonies infested with the parasitic mite Varroa jacobsoni. Annals of Applied Biology, 113: 27-244.

BARTHELL, JF; JM RANDALL; RW THORP & AM WENNER. 2001. Promotion of seed set in yellow star-thistle by honey bees: evidence of an invasive mutualism. Ecological Applications, 11: 1870–1883.

BROWN, MJF; R LOOSLI & P SCHMID-HEMPEL. 2000. Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos, 91: 421-427.

BROWN, MJF; R SCHMID-HEMPEL & P SCHMID-HEMPEL. 2003. Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. Journal of Animal Ecology, 72: 994-1002.

BUCHMANN, SL 1983. Buzz pollination in angiosperms. Pp. 73-113 in: CE Jones & RJ Little (eds.) Handbook of experimental pollination biology. Van Norstrand-Rheinhold, NewYork.

BUTTERMORE, RE; N POMEROY; W HOBSON; T SEMMENS & R HART. 1998. Assessment of the genetic base of Tasmanian bumble bees (Bombus terrestris) for development as pollination agents. Journal of Apicultural Research, 37: 23-25.

CANE, J. En prensa. An effective, Manageable Bee for pollination of Rubus Cane Fruits, Osmia aglaia. Acta Horticulturae.

CHACOFF, N & MA AIZEN. 2006. Edge effects on flower-visiting insects in grape fruit plantations bordering premontane subtropical forests. Journal of Applied Ecology, 43: 18-27.

CHAPMAN, RE & AFG BOURKE. 2001. The influence of sociality on the conservation biology of social insects. Ecology Letters, 4: 650-662.

COLLA, SR; MC OTTERSTATTER; RJ GEGEAR & JD THOMSON. 2006. Plight of the bumble bee: Pathogen spillover from commercial to wild populations. Biological Conservation, 129: 461-467.

DAFNI, A & A SHMIDA. 1996. The possible ecological implications of the invasion of Bombus terrestris (L.) (Apidae) at Mt Carmel, Israel. Pp. 84–199 in: Matheson A, Buchmann SL, O’Toole C, Westrich P, Williams IH (eds.). The Conservation of Bees. The Linnean Society of London and the International Bee Research Association, London

DURRER, S & P SCHMID-HEMPEL. 1994. Shared use of flowers leads to horizontal pathogen transmission. Proc R. Soc. Lond., B 258: 299-302.

FUSSELL, M & SA CORBET. 1991. Forage for bumblebees and honeybees in farmland: a case study. Journal of Apicultural Research, 30: 87-97.

GREENLEAF, S & C KREMEN. 2006. Wild bee species increase tomato production and respond differently to surrounding land use in Northern California. Biological Conservation, 133:81-87.

GREER, L. 1999. Alternative pollinators: Native Bees. Horticultural Technical Note of the Appropriate Technology Transfer for Rural Areas. 14 pp.

GOKA, K; K OKABE; S NIWA & M YONEDA. 2000. Parasitic mite infection in introduced colonies of European bumblebees, Bombus terrestris. Japanese Journal of Applied Entomology and Zoology, 44: 47-50.

GOKA, K; K OKABE; M YONEDA & S NIWA. 2001. Bumblebee commercialization will cause worldwide migration of parasitic mites. Molecular Ecology, 10: 2095-2099.

GOKA, K; K OKABE & M YONEDA. 2006. Worldwide migration of parasitic mites as a result of bumblebee commercialization. Population Ecology, 48:285-291.

GOULSON, D. 2003a. Effects of introduced bees on native ecosystems. Annual Review of Ecology and Systematics, 34: 1–26.

GOULSON, D. 2003b. Bumblebees, behaviour and ecology. Oxford University Press, NewYork. 235 pp.

GOULSON, D; JC STOUT & KELLS AR. 2002. Do exotic bumblebees and honeybees compete with native flower-visiting insects in Tasmania? Journal of Insects Conservation, 6: 179–189.

GOULSON, D & ME HANLEY. 2004. Distribution and forage use of exotic bumblebees in South Island, New Zealand. New Zealand Journal of Ecology, 28: 225–232.

HANLEY, ME & D GOULSON. 2003. Introduced weeds pollinated by introduced bees: Cause or effect? Weed Biology and Management, 3: 204–212.

HEINRICH, B. 1979. Bumblebee economics. 3 rd Edition, Harvard University Press, London, 245 pp.

HINGSTON, AB. 2005. Does the recently introduced bumblebee Bombus terrestris (Apidae) prefer flowers of introduced or native plants in Australia? Australian Journal of Zoology, 53: 29–34.

HINGSTON, AB & PB MCQUILLAN. 1998: Nectar robbing in Epacris impressa (Epacridaceae) by the recently introduced bumblebee Bombus terrestris (Apidae) in Tasmania. The Vict. Nat., 115: 116-119.

HINGSTON, AB & PB MCQUILLAN. 1999. Displacement of Tasmanian native Megachilid bees by the recently introduced bumblebee Bombus terrestris (Linnaeus, 1758) (Hymenoptera: Apidea). Austral Journal Zoology, 47: 59–65.

INARI, N; T NAGAMITSU; T KENTA; K GOKA & T HIURA. 2005. Spatial and temporal pattern of introduced Bombus terrestris abundance in Hokkaido, Japan, and its potential impact on native bumblebees. Population Ecology, 47: 77–82.

INGS, TC; SCHIKORA J & L CHITTKA. 2005. Bumblebees, humble pollinators or assiduous invaders? A population comparison of foraging performance in Bombus terrestris. Oecologia, 144: 508-516.

INGS, TC, NL WARD & L CHITTKA. 2006. Can commercially imported bumble bees out-compete their native conspecifics? Journal of Applied Ecology, 43: 940-948.

KENTA, T; N INARI, T NAGAMITSU; K GOKA & T HIURA. 2007. Commercialized European bumblebee can cause pollination disturbance: An experiment on seven native plant species in Japan. Biological Conservation, 134: 298-309.

KLEIN, AM; BE VAISSIERE; JH CANE; I STEFFAN- DEWENTER; SA CUNNINGHAM; C KREMEN & T TSCHARNTKE. 2007. Importance of pollinators in changing andscapes for world crops. Proceedings of the Royal Society, 274, 303-313.

KREMEN, C & T RICKETTS. 2000. Global perspectives on pollination disruptions. Conservation Biology, 14: 1226-1228.

KREMEN, C; NM WILLIAMS & RW THORP. 2004a. Crop pollination from native bees at risk from agricultural intensification. Proceedings of the National Academy of Science, 99: 16812-16816.

KREMEN, C; NM WILLIAMS; RL BUGG; JP FAY & RW THORP. 2004b. The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecology Letters, 7: 1109-1119.

KRAUSS, G. 1993. Preference of Varroa jacobsoni for honey bees (Apis mellifera) of different ages. Journal of Apicultural Research, 32: 57-64.

MALOOF, JE. 2001: The effects of a bumblebee nectar robber on plant reproductive success and pollinator behavior. Amer. J. Bot., 88: 1960-1965.

MALOOF, JE & DW INOUYE. 2000. Are nectar robber cheaters or mutualists? Ecology, 81: 2561-2661.

MACFARLANE, RP & L GURR. 1995. Distribution of bumblebees in New Zealand. New Zealand Entomologist, 18: 29–36.

MADJIDIAN, J. 2005. Impact of a potential replacement of the native bumblebee Bombus dahlbomii by the invasive Bombus ruderatus on the pollination of the native herb Alstroemeria aurea in Northern Patagonia, Argentina. Tesis de Maestría, Universidad de Lund, Suecia.

MALOOF, JE & DW INOUYE. 2000. Are nectar robber cheaters or mutualists? Ecology, 81: 2561-2661.

MARTIN, SJ. 2001. The role of Varroa and viral pathogens in the collapse of honey bee colonies: A modeling approach. Journal of Applied Ecology, 38: 1082-1093.

MEMMOTT, J; PG CRAZE; HM HARMAN; P SYRETT & SV FOWLER. 2005. The effect of propagule size on the invasion of an alien insect. Journal of Animal Ecology, 74: 50-62.

MOLLER, H. 1996. Lessons for invasion theory from social insects. Biol. Conserv., 78: 125-142.

MORALES, CL. 2006. Alteración del hábitat e interacciones entre especies nativas y exóticas a través de la polinización en Bosques Templados de Sudamérica Austral. Tesis Doctoral. Universidad Nacional del Comahue, Bariloche, Argentina.

MORALES, CL & MA AIZEN. 2002. Does the invasion of alien plants promote invasion of alien flower visitors? A case study from the temperate forests of southern Andes. Biological Invasions, 4: 87–100.

MORALES, CL & MA AIZEN. 2006. Invasive mutualisms and the structure of plant–pollinator interactions in the temperate forests of north-west Patagonia, Argentina. Journal of Ecology, 94: 171–180.

MORALES, CL & MA AIZEN. 2006. Informe sobre la solicitud de Autorización de Bombus impatiens a Argentina. Presentado a solicitud de SENASA- Argentina. (Servicio Nacional de Sanidad y Calidad Agroalimentaria), 30 pp.

MORANDIN, LA; T M LAVERTY; PGG KEVAN; S KHOSLA & L SHIPP. 2001. Bumble bee (Hymenoptera: Apidae) activity and loss in commercial tomato greenhouses. Canadian Entomologist, 133:883-893.

NAGAMITSU, T; T KENTA; N INARI; E KATO & T HIURA. 2007. Abundance, body size, and morphology of bumblebees in an area where an exotic species, Bombus terrestris, has colonized in Japan. Ecological Research, 22:331-341.

PAINI, DR. 2004. Impact of honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: A review. Austral Ecology, 29: 399–407.

REBOLLEDO, RR; HP MARTINEZ; MR PALMA; AP AGUILERA & CK KLEIN. 2004. Actividad de visita de Bombus dahlbomii (Guérin) y Bombus ruderatus (F.) (Himenoptera: Apidae) sobre trébol rosado (Trifolium pratense L.). Agricultura Técnica (Chile) 64: 245–250.

ROIG-ALSINA, A & MA AIZEN. 1996. Bombus ruderatus Fabricius, un nuevo Bombus para la Argentina (Hymenoptera: Apidea). Physis, 5: 49–50.

ROUBIK, D. 1978. Competitive interactions between neotropical pollinators and africanized honey bees. Science, 201: 2030–2032.

ROUBIK, DW. 1983. Experimental community studies: time-series tests of competition between African and neotropical bees. Ecology, 64: 971-978.

ROUBIK, DW. 2001. Ups and downs in pollinator populations: When is there a decline? Conservation Ecology 5(1): 2. [online] URL: http://www.consecol.org/vol5/iss1/art2

RUIZ-GONZÁLEZ, MX & MJF BROWN. 2006. Honeybee and bumblebee trypanosomatids: specificity and potential for transmission. Ecological Entomology, 31: 616-622.

RUZ, L. 2002. Bee pollinators introduced to Chile: A review. Pp. 155–167 in: PG Kevan y VL Imperatriz-Fonseca (eds.) Pollinating Bees. The Conservation Link between Agriculture and Nature. Proceedings of the workshop on the Conservation and Sustainable Use of Pollinators in Agriculture, with emphasis on Bees. Brasilia.

RUZ, L & R HERRERA. 2001. Preliminary Observations on Foraging activities of Bombus dahlbomii and Bombus terrestris (Hym: Apidae) on native and non-native vegetation in Chile. Act. Hort., 561: 165-169.

SCHMID-HEMPEL, P. 1998. Parasites in social insects. Princeton University Press, New Jersey.

SCHMID-HEMPEL, P & R LOOSLI. 1998. A contribution to the knowledge of Nosema infections in bumblebees, Bombus spp. Apidologie, 29: 525-535.

SEMMENS, TD; E TURNER & R BUTTERMORE. 1993. Bombus terrestris (L.) (Hymenoptera: Paidae) now established in Tasmania. Journal of the Australian Entomological Society, 32: 346.

SIMBERLOFF, D & B VON HOLLE. 1999. Positive interactions of nonindigenous species: invasional meltdown? Biological Invasions, 1: 21–32.

SLAA, EJ; LA SANCHEZ CHAVES; KS MALAGODI-BRAGA & FE HOFSTEDE. 2006. Stingless bees in applied pollination: practice and perspectives. Apidologie, 37: 293-315.

SPIEWOK, S & P NEUMANN. 2006. Infestation of commercial bumblebee (Bombus impatiens) field colonies by small hive beetles (Aethinia tumida). Ecological Entomology 312: 623-628.

STOUT, JC. 2000. Do size matter? Bumblebee behavior and the pollination of Cytisus scoparius L. (Fabaceae). Apidologie, 31: 129-139.

STOUT, JC & D GOULSON. 2000. Bumble bees in Tasmania: their distribution and potential impact on Australian flora and fauna. Bee World, 81: 80–86.

STOUT, JC; AR KELLS & D GOULSON. 2002. Pollination of the invasive shrub Lupinus arboreus (Fabaceae) by introduced bees in Tasmania. Biological Conservation, 106: 425–434.

THOMSON, D. 2004. Competitive interactions between the invasive European honey bee and native bumblebees. Ecology, 85: 458–470.

THOMSON, D. 2006. Detecting the effects of introduced species: a case study of competition between Apis and Bombus. Oikos, 114: 407-418.

THORP, RW. 2003. Bumble bees (Hymenoptera: Apidae): Commercial Use and Environmental Concerns. Pp. 21-40 in: K Strickler and JH Cane (eds.). For nonnative crops, whence pollinators of the future? Thomas Say Publications in Entomology: Proceedings. Enthomological Society of America, Lanham, MD.

TORRETA, JP; D MEDAN & AH ABRAHAMOVICH. 2006. First record of the invasive bumblebee Bombus terrestris (L.) (Hymenoptera, Apidae) in Argentina. Transactions of the American Entomological Society, 132: 285-289.

URCELAY, C; C MORALES & V CHALCOFF. 2006. Relationship between corolla length and floral larceny in the South American hummingbird pollinated Campsidium valdivianum (Bignoniaceae). Ann. Bot. Fennici, 4: 205-211.

VELTHUIS, HHW. 2002. The historical background of the domestication of the bumble-bee, Bombus terrestris, and its introduction in agriculture. Pp 177-184 in: Kevan P, Imperatriz Fonseca VL (eds) Pollinating Bees- the conservation link between agriculture and nature. Ministry of Environment, Brazil,

VELTHUIS, H HW & A VAN DOORN. 2006. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie, 37: 421-451.

VERGARA, CH. En prensa. Environmental Impact of Exotic Bees introduced for Crop pollination. En: The Impact of Bees on Agricultural Systems. Oxford University Press.

VON HOLLE, B & D SIMBERLOFF. 2005. Ecological resistance to biological invasion overwhelmed by propagule pressure. Ecology, 86: 3212-3218.

WESTPHAL, C; IS DEWENTER & T TSCHARNTKE. 2003. Mass flowering crops enhance pollinato densities at landscape scale. Ecology Letters, 6, 961-965.

WHITTINGTON, R & ML WINSTON. 2003. Effects of Nosema bombi and its treatment fumagillin on bumble bee (Bombus occidentalis) colonies. Journal of Invertebrate Pathology, 84:54-58.

WHITTINGTON, R & ML WINSTON. 2004. Comparison and examination of Bombus occidentalis and Bombus impatiens (Hymenoptera: Apidae) in tomato greenhouses. Journal of Economic Entomology, 97: 1384-1389.

WILLIAMS, PH. 1998. An annotated checklist of bumble bees with an analysis of patterns of description (Hymenoptera: Apidae, Bombini). Bulletin of The Natural History Museum (Entomology), 67: 79-152.

WILLMER, PG; AAM BATAW & JP HIGHES. 1994. The superiority of bumblebees to honeybees as pollinators: insect visits to raspberry flowers. Ecological Entomology, 9: 271-284.

WINTER, K; L ADAMS; R THORP; D INOUYE; L DAY; J ASCHER & S BUCHMANN. 2006. Importation of non-native Bumble bees into North America: Potential consequences of using Bombus terrestris and other non-native bumblebees for Greenhouse Crop Pollination in Canada, Mexico, and the United States. White Paper of the North American Pollinator Protection Campaign. 33 pp.
Publicado
2007-06-01
Sección
Sección Especial