Mito y realidad de una crisis global de la polinización en la agricultura

Autores/as

  • Marcelo A. Aizen Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA), Universidad Nacional del Comahue-CONICET. San Carlos de Bariloche, Rio Negro, Argentina. Wissenschaftskolleg zu Berlin. Berlin, Germany
  • Lucas A. Garibaldi Universidad Nacional de Río Negro. Instituto de Investigaciones en Recursos Naturales, Agroecología y Desarrollo Rural. Río Negro, Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. Instituto de Investigaciones en Recursos Naturales, Agroecología y Desarrollo Rural. Río Negro, Argentina
  • Lawrence D. Harder Department of Biological Sciences, University of Calgary. Calgary, Alberta, Canada

DOI:

https://doi.org/10.25260/EA.22.32.2.1.1875

Palabras clave:

agricultura, cereales, frutales, abejas melíferas, oleaginosas, crisis de polinización, declive de los polinizadores, dependencia de los polinizadores, raíces y tubérculos

Resumen

Los polinizadores están disminuyendo como consecuencia de la degradación generalizada del medio ambiente. Esta pérdida ha suscitado la preocupación de que una crisis global de polinización pueda estar amenazando nuestro suministro de alimentos vía una reducción en el rendimiento agrícola. Sin embargo, tres líneas de evidencia no apoyan tal expectativa. Primero, aunque la abundancia y la diversidad de los polinizadores silvestres están disminuyendo en todo el mundo, la población mundial de colmenas de abejas melíferas manejadas ha aumentado en un ~80% desde principios de la década de 1960. Segundo, la producción agrícola disminuiría sólo <10% en ausencia total de abejas ya que relativamente pocos cultivos dependen completamente de los polinizadores. Por último, a nivel global no parece existir una desaceleración del crecimiento en el rendimiento con el incremento en la dependencia de los polinizadores. Sin embargo, la expansión de cultivos dependientes de polinizadores puede tener un alto costo ambiental. Aunque los polinizadores son responsables de una fracción menor de la producción agrícola mundial, esta fracción ha aumentado en un ~600% desde 1961, superando el crecimiento de la población mundial de abejas melíferas manejadas. El incremento de esta fracción de la agricultura se explica en gran medida por la rápida expansión de monocultivos dependientes de polinizadores. A través de incrementar la pérdida de polinizadores silvestres, esta transformación en el uso de la tierra puede causar un incremento en los déficits de polinización y promover la expansión de cultivos dependientes de polinizadores en respuesta a demandas sostenidas del mercado. Por lo tanto, una espiral de retroalimentación positiva entre la expansión de la agricultura y un declive de los polinizadores que afecte al rendimiento de los cultivos podría acelerar la enorme pérdida de biodiversidad en curso al promover la destrucción de los hábitats naturales remanentes y la homogeneización de los paisajes agrícolas.

Citas

Aizen, M. A., and P. Feinsinger. 2003. Bees not to be? Responses of insect pollinator faunas and flower pollination to habitat fragmentation. Pp. 111-129 in G. A. Bradshaw, P. A. Marquet and K. L. Ronnenberg (eds.). How landscapes change: human disturbance and ecosystem disruptions in the Americas. Springer, New York. https://doi.org/10.1007/978-3-662-05238-9_7.

Aizen, M. A., and L. D. Harder. 2007. Expanding the limits of the pollen‐limitation concept: effects of pollen quantity and quality. Ecology 88:271-281. https://doi.org/10.1890/06-1017.

Aizen, M. A., L. A. Garibaldi, S. A. Cunningham, and A. M. Klein. 2008. Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Current Biology 18:1572-1575. https://doi.org/10.1016/j.cub.2008.08.066.

Aizen, M. A., L. A. Garibaldi, S. A. Cunningham, and A. M. Klein. 2009. How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Annals of Botany 103:1579-1588. https://doi.org/10.1093/aob/mcp076.

Aizen, M. A., and L. D. Harder. 2009a. The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Current Biology 19:915-918. https://doi.org/10.1016/j.cub.2009.03.071.

Aizen, M. A., and L. D. Harder. 2009b. Geographic variation in the growth of domesticated honey-bee stocks. Communicative and Integrative Biology 2:464-466. https://doi.org/10.4161/cib.2.6.9258.

Aizen, M. A., C. L. Morales, D. P. Vázquez, L. A. Garibaldi, A. Sáez, and L. D. Harder. 2014. When mutualism goes bad: density-dependent impacts of introduced bees on plant reproduction. New Phytologist 204:322-328. https://doi.org/10.1111/nph.12924.

Aizen, M. A., S. Aguiar, J. C. Biesmeijer, L. A. Garibaldi, D. W. Inouye, C. Jung, D. J. Martins, R. Medel, C. L. Morales, H. Ngo, A. Pauw, R. J. Paxton, A. Sáez, and C. L. Seymour. 2019a. Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification. Global Change Biology 25:3516-3527. https://doi.org/10.1111/gcb.14736.

Aizen, M. A., C. Smith-Ramírez, C. L. Morales, L. Vieli, A. Sáez, R. M. Barahona-Segovia, M. P. Arbetman, J. Montalva, L. A. Garibaldi, D. W. Inouye, and L. D. Harder. 2019b. Coordinated species importation policies are needed to reduce serious invasions globally: the case of alien bumblebees in South America. Journal of Applied Ecology 56:100-106. https://doi.org/10.1111/1365-2664.13121.

Aizen, M. A., M. P. Arbetman, N. P. Chacoff, V. R. Chalcoff, P. Feinsinger, L. A. Garibaldi, L. D. Harder, C. L. Morales, A. Sáez, and A. J. Vanbergen. 2020. Invasive bees and their impact on agriculture. Advances in Ecological Research 63:49-92. https://doi.org/10.1016/bs.aecr.2020.08.001.

Albrecht, M., B. Schmid, Y. Hautier, and C. B. Müller. 2012. Diverse pollinator communities enhance plant reproductive success. Proceedings of the Royal Society B: Biological Sciences 279:4845-4852. https://doi.org/10.1098/RSPB.2012.1621.

Alsahlany, M., F. Enciso-Rodríguez, M. López-Cruz, J. Coombs, and D. S. Douches. 2021. Developing self-compatible diploid potato germplasm through recurrent selection. Euphytica 217:1-16. https://doi.org/10.1007/s10681-021-02785-0.

Allen-Wardell, G., P. Bernhardt, R. Bitner, A. Burquez, S. Buchmann, J. Cane, P. A. Cox, V. Dalton, P. Feinsinger, M. Ingram, D. Inouye, C. E. Jones, K. Kennedy, P. Kevan, H. Koopowitz, R. Medellin, S. Medellin-Morales, G. P. Nabhan, B. Pavlik, V. Tepedino, P. Torchio, and S. Walker. 1998. The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conservation Biology 12:8-17. https://doi.org/10.1046/j.1523-1739.1998.97154.x.

Arbetman, M. P., I. Meeus, C. L. Morales, M. A. Aizen, and G. Smagghe. 2012. Alien parasite hitchhikes to Patagonia on invasive bumblebee. Biological Invasions 15:489-494. https://doi.org/10.1007/s10530-012-0311-0.

Bates, D., M. Mächler, B. M. Bolker, and S. C. Walker. 2015. Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67:1-48. https://doi.org/10.18637/jss.v067.i01.

Biesmeijer, J. C., S. P. M. Roberts, M. Reemer, R. Ohlemuller, M. Edwards, T. Peeters, A. P. Schaffers, S. G. Potts, R. Kleukers, and C. D. Thomas. 2006. Parallel declines in pollinators and insect pollinated plants in Britain and the Netherlands. Science 313:351-354. https://doi.org/10.1126/science.1127863.

Blacquière, T., G. Smagghe, C. A. M. Van Gestel, and V. Mommaerts. 2012. Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973-992. https://doi.org/10.1007/s10646-012-0863-x.

Buchholz, S., A. K. Gathof, A. J. Grossmann, I. Kowarik, and L. K. Fischer. 2020. Wild bees in urban grasslands: urbanisation, functional diversity and species traits. Landscape and Urban Planning 196:103731. https://doi.org/10.1016/j.landurbplan.2019.103731.

Buchmann, S. L., and G. P. Nabhan. 1996. The forgotten pollinators. Isla Press, Washington DC, USA.

Cameron, S. A., J. D. Lozier, J. P. Strange, J. B. Koch, N. Cordes, L. F. Solter, T. L. Griswold, and G. E. Robinson. 2011. Patterns of widespread decline in North American bumble bees. Proceedings of the National Academy of Sciences 108:662-667. https://doi.org/10.1073/pnas.1014743108.

Cardinale, B. J., J. E. Duffy, A. González, D. U. Hooper, C. Perrings, P. Venail, A. Narwani, G. M. Mace, D. Tilman, D. A Wardle, A. P. Kinzig, G. C. Daily, M. Loreau, J. B. Grace, A. Larigauderie, D. S. Srivastava, and S. Naeem. 2012. Biodiversity loss and its impact on humanity. Nature 486:59-67. https://doi.org/10.1038/nature11148.

Chaplin-Kramer, R., E. Dombeck, J. Gerber, K. A. Knuth, N. D. Mueller, M. Mueller, G. Ziv, and A. M. Klein. 2014. Global malnutrition overlaps with pollinator-dependent micronutrient production. Proceedings of the Royal Society B: Biological Sciences 281:20141799. https://doi.org/10.1098/rspb.2014.1799.

Chaudhary, A., and T. M. Brooks. 2019. National consumption and global trade impacts on biodiversity. World Development 121:178-187. https://doi.org/10.1016/j.worlddev.2017.10.012.

Cheptou, P.-O. 2021. Pollination strategies in the face of pollinator decline. Botany Letters. https://doi.org/10.1080/23818107.2021.1884900.

Colla, S. R., F. Gadallah, L. Richardson, D. Wagner, and L. Gall. 2012. Assessing declines of North American bumble bees (Bombus spp.) using museum specimens. Biodiversity and Conservation 21:3585-3595. https://doi.org/10.1007/s10531-012-0383-2.

Corley, R. H. V., and P. B. Tinker. 2016. The oil palm. 5th edition. Wiley, Chichester, UK. https://doi.org/10.1002/9781118953297.

Dauvergne, P. 2008. The shadows of consumption: consequences for the global environment. MIT Press, Cambridge, MA, USA. https://doi.org/10.7551/mitpress/7706.001.0001.

Deguines, N., C. Jono, M. Baude, M. Henry, R. Julliard, and C. Fontaine. 2014. Large-scale trade-off between agricultural intensification and crop pollination services. Frontiers in Ecology and the Environment 12:212-217. https://doi.org/10.1890/130054.

Desneux, N., A. Decourtye, and J. M. Delpuech. 2007. The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology 52:81-106. https://doi.org/10.1146/annurev.ento.52.110405.091440.

Devillers, J., and H. Devillers. 2020. Lethal and sublethal effects of pyriproxyfen on Apis and non-Apis bees. Toxics 8:1-21. https://doi.org/10.3390/toxics8040104.

Díaz, S., J. Fargione, F. S. Chapin, and D. Tilman. 2006. Biodiversity loss threatens human well-being. PLoS Biology 4:e277. https://doi.org/10.1371/journal.pbio.0040277.

Dicks, L. V., T. D. Breeze, H. T. Ngo, D. Senapathi, J. An, M. A. Aizen, P. Basu, D. Buchori, L. Galetto, L. A. Garibaldi, B. Gemmill-Herren, B. G. Howlett, V. L. Imperatriz-Fonseca, S. D. Johnson, A. Kovács-Hostyánszki, Y. J. Kwon, H. M. G. Lattorff, T. Lungharwo, C. L. Seymour, A. J. Vanbergen, and S. G. Potts. 2021. A global-scale expert assessment of drivers and risks associated with pollinator decline. Nature, Ecology and Evolution. https://doi.org/10.1038/s41559-021-01534-9.

Eilers, E. J., C. Kremen, S. S. Greenleaf, A. K. Garber, and A. M. Klein. 2011. Contribution of pollinator-mediated crops to nutrients in the human food supply. PLoS ONE 6:e21363. https://doi.org/10.1371/journal.pone.0021363.

Ellis, A. M., S. S. Myers, and T. H. Ricketts. 2015. Do pollinators contribute to nutritional health? PLoS ONE 10:e114805. https://doi.org/10.1371/journal.pone.0114805.

FAOSTAT. 2021. Data available at http://www.fao.org/faostat/en/#home. Accessed July 1-7-2021.

Fehlenberg, V., M. Baumann, N. I. Gasparri, M. Piquer-Rodriguez, G. Gavier-Pizarro, and T. Kuemmerle. 2017. The role of soybean production as an underlying driver of deforestation in the South American Chaco. Global Environmental Change 45:24-34. https://doi.org/10.1016/j.gloenvcha.2017.05.001.

Fitzherbert, E. B., M. J. Struebig, A. Morel, F. Danielsen, C. A. Brühl, P. F. Donald, and B. Phalan. 2008. How will oil palm expansion affect biodiversity? Trends in Ecology and Evolution 23:538-545. https://doi.org/10.1016/j.tree.2008.06.012.

Gallai, N., J.-M. M. Salles, J. Settele, and B. E. Vaissière. 2009. Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecological Economics 68:810-821. https://doi.org/10.1016/j.ecolecon.2008.06.014.

Garibaldi, L. A., M. A. Aizen, S. A. Cunningham, and A. M. Klein. 2009. Pollinator shortage and global crop yield: looking at the whole spectrum of pollinator dependency. Communicative and Integrative Biology 2:37-39. https://doi.org/10.1016/jcub.200808066.

Garibaldi, L. A., M. A. Aizen, A. M. Klein, S. A. Cunningham, and L. D. Harder. 2011a. Global growth and stability of agricultural yield decrease with pollinator dependence. Proceedings of the National Academy of Sciences 108:5909-5914. https://doi.org/10.1073/pnas.1012431108.

Garibaldi, L. A., I. Steffan-Dewenter, C. Kremen, J. M. Morales, R. Bommarco, S. A. Cunningham, L. G. Carvalheiro, N. P. Chacoff, J. H. Dudenhöffer, S. S. Greenleaf, A. Holzschuh, R. Isaacs, K. Krewenka, Y. Mandelik, M. M. Mayfield, L. A. Morandin, S. G. Potts, T. H. Ricketts, H. Szentgyörgyi, B. F. Viana, C. Westphal, R. Winfree, and A. M. Klein. 2011b. Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecology Letters 14:1062-1072. https://doi.org/10.1111/j.1461-0248.2011.01669.x.

Garibaldi, L. A., I. Steffan-Dewenter, R. Winfree, M. A. Aizen, R. Bommarco, S. A. Cunningham, C. Kremen, L. G. Carvalheiro, L. D. Harder, O. Afik, I. Bartomeus, F. Benjamin, V. Boreux, D. Cariveau, N. P. Chacoff, J. H. Dudenhöffer, B. M. Freitas, J. Ghazoul, S. Greenleaf, J. Hipólito, A. Holzschuh, B. Howlett, R. Isaacs, S. K. Javorek, C. M. Kennedy, K. M. Krewenka, S. Krishnan, Y. Mandelik, M. M. Mayfield, I. Motzke, T. Munyuli, B. A. Nault, M. Otieno, J. Petersen, G. Pisanty, S. G. Potts, R. Rader, T. H. Ricketts, M. Rundlöf, C. L. Seymour, C. Schüepp, H. Szentgyörgyi, H. Taki, T. Tscharntke, C. H. Vergara, B. F. Viana, T. C. Wanger, C. Westphal, N. Williams, and A. M. Klein. 2013. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608-1611. https://doi.org/10.1126/science.1230200.

Garibaldi, L. A., L. G. Carvalheiro, S. D. Leonhardt, M. A. Aizen, B. R. Blaauw, R. Isaacs, M. Kuhlmann, D. Kleijn, A. M. Klein, C. Kremen, L. Morandin, J. Scheper, and R. Winfree. 2014. From research to action: enhancing crop yield through wild pollinators. Frontiers in Ecology and the Environment 12:439-447. https://doi.org/10.1890/130330.

Garibaldi, L. A., L. G. Carvalheiro, B. E. Vaissière, B. Gemmill-Herren, J. Hipólito, B. M. Freitas, H. T. Ngo, N. Azzu, A. Sáez, J. Åström, J. An, B. Blochtein, D. Buchori, F. J. Chamorro García, F. O. Da Silva, K. Devkota, M. De Fátima Ribeiro, L. Freitas, M. C. Gaglianone, M. Goss, M. Irshad, M. Kasina, A. J. S. Pacheco Filho, L. H. Piedade Kiill, P. Kwapong, G. N. Parra, C. Pires, V. Pires, R. S. Rawal, A. Rizali, A. M. Saraiva, R. Veldtman, B. F. Viana, S. Witter, and H. Zhang. 2016. Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms. Science 351:388-391. https://doi.org/10.1126/science.aac7287.

Garibaldi, L. A., N. Pérez‐Méndez, G. D. Cordeiro, A. Hughes, M. Orr, I. Alves‐dos‐Santos, B. M. Freitas, F. Freitas de Oliveira, G. LeBuhn, I. Bartomeus, M. A. Aizen, P. B. Andrade, B. Blochtein, D. Boscolo, P. M. Drumond, M. C. Gaglianone, B. Gemmill‐Herren, R. Halinski, C. Krug, M. M. Maués, L. H. Piedade Kiill, M. Pinheiro, C. S. S. Pires, and B. F. Viana. 2021. Negative impacts of dominance on bee communities: does the influence of invasive honey bees differ from native bees? Ecology 102:e03526. https://doi.org/10.1002/ecy.3526.

Gasparri, N. I., H. R. Grau, and J. Gutiérrez Angonese. 2013. Linkages between soybean and neotropical deforestation: coupling and transient decoupling dynamics in a multi-decadal analysis. Global Environmental Change 23:1605-1614. https://doi.org/10.1016/j.gloenvcha.2013.09.007.

Ghazoul, J. 2005. Buzziness as usual? Questioning the global pollination crisis. Trends in Ecology and Evolution 20:367-373. https://doi.org/10.1016/j.tree.2005.04.026.

Gleiser, G., N. L. Da Cunha, A. Sáez, and M. A. Aizen. 2021. Ecological correlates of crop yield growth and interannual yield variation at a global scale. Web Ecology 21:15-43. https://doi.org/10.5194/we-21-15-2021.

Goulson, D. 2010. Bumblebees: behaviour, ecology, and conservation. 2nd edition. Oxford University Press, Oxford, UK.

Goulson, D., G. C. Lye, and B. Darvill. 2008. Decline and conservation of bumble bees. Annual Review of Entomology 53:191-208. https://doi.org/10.1146/annurev.ento.53.103106.093454.

Greenleaf, S. S., and C. Kremen. 2006. Wild bees enhance honey bees’ pollination of hybrid sunflower. Proceedings of the National Academy of Sciences 103:13890-13895. https://doi.org/10.1073/PNAS.0600929103.

Harder, L. D., and M. B. Routley. 2006. Pollen and ovule fates and reproductive performance by flowering plants. Pp. 61-80 in L. D. Harder and S. C. H. Barrett (eds.). Ecology and evolution of flowers. Oxford University Press, Oxford, UK.

Harder, L. D., and M. A. Aizen. 2010. Floral adaptation and diversification under pollen limitation. Philosophical transactions of the Royal Society of London. Series B, Biological Sciences 365:529-543. https://doi.org/10.1098/rstb.2009.0226.

Harder, L. D., M. A. Aizen, S. A. Richards, M. A. Joseph, and J. W. Busch. 2016. Diverse ecological relations of male gametophyte populations in stylar environments. American Journal of Botany 103:484-497. https://doi.org/10.3732/ajb.1500269.

Hargreaves, A. L., L. D. Harder, and S. D. Johnson. 2009. Consumptive emasculation: the ecological and evolutionary consequences of pollen theft. Biological Reviews 84:259-276. https://doi.org/10.1111/j.1469-185X.2008.00074.x.

Herrera, C. M. 2020. Gradual replacement of wild bees by honeybees in flowers of the Mediterranean Basin over the last 50 years. Proceedings of the Royal Society B: Biological Sciences 287:20192657. https://doi.org/10.1101/828160.

Hung, K. L. J., J. M. Kingston, M. Albrecht, D. A. Holway, and J. R. Kohn. 2018. The worldwide importance of honey bees as pollinators in natural habitats. Proceedings of the Royal Society B: Biological Sciences 285:20172140. https://doi.org/10.1098/rspb.2017.2140.

IPBES. 2016. The assessment report on pollinators, pollination and food production of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. S. G. Potts, V. L. Imperatriz-Fonseca and H. T. Ngo (eds.). Secretariat of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services, Bonn, Germany. https://doi.org/10.5281/zenodo.3402856.

IPBES. 2019. Global assessment report on biodiversity and ecosystem services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services. E. S. Brondizio, J. Settele, S. Díaz and H. T. Ngo (eds.). Secretariat of the Intergovernmental Science-Policy Platform, Bonn, Germany. https://doi.org/10.5281/zenodo.3831673.

Hladik, M. L., A. R. Main, and D. Goulson. 2018. Environmental risks and challenges associated with neonicotinoid insecticides. Environmental Science and Technology 52:3329-3335. https://doi.org/10.1021/acs.est.7b06388.

Jones, A. D. 2017. Critical review of the emerging research evidence on agricultural biodiversity, diet diversity, and nutritional status in low-and middle-income countries. Nutrition Reviews 75:769-782. https://doi.org/10.1093/nutrit/nux040.

Kastner, T., M. J. I. Rivas, W. Koch, and S. Nonhebel. 2012. Global changes in diets and the consequences for land requirements for food. Proceedings of the National Academy 109:6868-6872. https://doi.org/10.1073/pnas.1117054109.

Kerr, J. T., A. Pindar, P. Galpern, L. Packer, S. G. Potts, S. M. Roberts, P. Rasmont, O. Schweiger, S. R. Colla, L. L. Richardson, D. L. Wagner, L. F. Gall, D. S. Sikes, and A. Pantoja. 2015. Climate change impacts on bumblebees converge across continents. Science 349:177-180. https://doi.org/10.1126/science.aaa7031.

King, C., G. Ballantyne, and P. G. Willmer. 2013. Why flower visitation is a poor proxy for pollination: measuring single-visit pollen deposition, with implications for pollination networks and conservation. Methods in Ecology and Evolution 4:811-818. https://doi.org/10.1111/2041-210X.12074.

Klein, A.-M., B. E. Vaissière, J. H. Cane, I. Steffan-Dewenter, S. A. Cunningham, C. Kremen, and T. Tscharntke. 2007. Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences 274:303-313. https://doi.org/10.1098/rspb.2006.3721.

Klopfenstein, T. J., G. E. Erickson, and L. L. Berger. 2013. Maize is a critically important source of food, feed, energy and forage in the USA. Field Crops Research 153:5-11. https://doi.org/10.1016/j.fcr.2012.11.006.

Knight, T. M., J. A. Steets, J. C. Vamosi, S. J. Mazer, M. Burd, D. R. Campbell, M. R. Dudash, M. O. Johnston, R. J. Mitchell, and T. L. Ashman. 2005. Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution, and Systematics 36:467-497. https://doi.org/10.1146/annurev.ecolsys.36.102403.115320.

Koh, L. P., and D. S. Wilcove. 2007. Cashing in palm oil for conservation. Nature 448:993-994. https://doi.org/10.1038/448993a.

Koski, M. H., J. L. Ison, A. Padilla, A. Q. Pham, and L. F. Galloway. 2018. Linking pollinator efficiency to patterns of pollen limitation: small bees exploit the plant-pollinator mutualism. Proceedings of the Royal Society B: Biological Sciences 285:20180635. https://doi.org/10.1098/rspb.2018.0635.

Kremen, C., N. M. Williams, M. A. Aizen, B. Gemmill-Herren, G. LeBuhn, R. Minckley, L. Packer, S. G. Potts, T. Roulston, I. Steffan-Dewenter, D. P. Vázquez, R. Winfree, L. Adams, E. E. Crone, S. S. Greenleaf, T. H. Keitt, A.-M. M. Klein, J. Regetz, and T. H. Ricketts. 2007. Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecology Letters 10:299-314. https://doi.org/10.1111/j.1461-0248.2007.01018.x.

Lautenbach, S., R. Seppelt, J. Liebscher, and C. F. Dormann. 2012. Spatial and temporal trends of global pollination benefit. PLoS ONE 7:e35954. https://doi.org/10.1371/journal.pone.0035954.

Lenzen, M., D. Moran, K. Kanemoto, B. Foran, L. Lobefaro, and A. Geschke. 2012. International trade drives biodiversity threats in developing nations. Nature 486:109-112. https://doi.org/10.1038/nature11145.

Mallinger, R. E., H. R. Gaines-Day, and C. Gratton. 2017. Do managed bees have negative effects on wild bees?: A systematic review of the literature. PLoS ONE 12:e0189268. https://doi.org/10.1371/journal.pone.0189268.

Miñarro, M., and D. García. 2018. Complementarity and redundancy in the functional niche of cider apple pollinators. Apidologie 49:789-802. https://doi.org/10.1007/s13592-018-0600-4.

Morales, C. L., M. P. Arbetman, S. A. Cameron, and M. A. Aizen. 2013. Rapid ecological replacement of a native bumble bee by invasive species. Frontiers in Ecology and the Environment 11:529-534. https://doi.org/10.1890/120321.

Murray, T. E., M. Kuhlmann, and S. G. Potts. 2009. Conservation ecology of bees: populations, species and communities. Apidologie 40:211-236. https://doi.org/10.1051/APIDO/2009015.

Nicholls, C. I., and M. A. Altieri. 2013. Plant biodiversity enhances bees and other insect pollinators in agroecosystems. A review. Agronomy for Sustainable Development 33:257-274. https://doi.org/10.1007/s13593-012-0092-y.

Normandin, É., N. J. Vereecken, C. M. Buddle, and V. Fournier. 2017. Taxonomic and functional trait diversity of wild bees in different urban settings. PeerJ 2017:e3051. https://doi.org/10.7717/peerj.3051.

Oldroyd, B. P. 2007. What’s killing American honey bees? PLoS Biology 5:1195-1199. https://doi.org/10.1371/journal.pbio.0050168.

Ollerton, J., H. Erenler, M. Edwards, and R. Crockett. 2014. Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science 346:1360-1362. https://doi.org/10.1126/science.1257259.

Ollerton, J., R. Winfree, and S. Tarrant. 2011. How many flowering plants are pollinated by animals? Oikos 120:321-326. https://doi.org/10.1111/j.1600-0706.2010.18644.x.

Osterman, J., M. A. Aizen, J. C. Biesmeijer, J. Bosch, B. G. Howlett, D. W. Inouye, C. Jung, D. J. Martins, R. Medel, A. Pauw, C. L. Seymour, and R. J. Paxton. 2021. Global trends in the number and diversity of managed pollinator species. Agriculture, Ecosystems and Environment 322:107653. https://doi.org/10.1016/j.agee.2021.107653.

Potts, S. G., J. C. Biesmeijer, C. Kremen, P. Neumann, O. Schweiger, and W. E. Kunin. 2010. Global pollinator declines: trends, impacts and drivers. Trends in Ecology and Evolution 25:345-353. https://doi.org/10.1016/j.tree.2010.01.007.

Potts, S. G., V. Imperatriz-Fonseca, H. T. Ngo, M. A. Aizen, J. C. Biesmeijer, T. D. Breeze, L. V. Dicks, L. A. Garibaldi, R. Hill, J. Settele, and A. J. Vanbergen. 2016. Safeguarding pollinators and their values to human well-being. Nature 540:220-229. https://doi.org/10.1038/nature20588.

Potts, S. G., P. Neumann, B. Vaissière, and N. J. Vereecken. 2018. Robotic bees for crop pollination: why drones cannot replace biodiversity. Science of the Total Environment 642:665-667. https://doi.org/10.1016/j.scitotenv.2018.06.114.

R Core Team. 2020. R: a language and environment for statistical computing. URL: R-project.org. R foundation for statistical computing, Vienna, Austria.

Rader, R., I. Bartomeus, L. A. Garibaldi, M. P. D. Garratt, B. G. Howlett, R. Winfree, S. A. Cunningham, M. M. Mayfield, A. D. Arthur, G. K. S. Andersson, R. Bommarco, C. Brittain, L. G. Carvalheiro, N. P. Chacoff, M. H. Entling, B. Foully, B. M. Freitas, B. Gemmill-Herren, J. Ghazoul, S. R. Griffin, C. L. Gross, L. Herbertsson, F. Herzog, J. Hipólito, S. Jaggar, F. Jauker, A.-M. Klein, D. Kleijn, S. Krishnan, C. Q. Lemos, S. A. M. Lindström, Y. Mandelik, V. M. Monteiro, W. Nelson, L. Nilsson, D. E. Pattemore, N. de O. Pereira, G. Pisanty, S. G. Potts, M. Reemer, M. Rundlöf, C. S. Sheffield, J. Scheper, C. Schüepp, H. G. Smith, D. A. Stanley, J. C. Stout, H. Szentgyörgyi, H. Taki, C. H. Vergara, B. F. Viana, and M. Woyciechowski. 2016. Non-bee insects are important contributors to global crop pollination. Proceedings of the National Academy of Sciences 113:146-151. https://doi.org/10.1073/pnas.1517092112.

Raven, P. H., and D. L. Wagner. 2021. Agricultural intensification and climate change are rapidly decreasing insect biodiversity. Proceedings of the National Academy of Sciences 118:e2002548117. https://doi.org/10.1073/PNAS.2002548117.

Richardson, L. L., K. P. McFarland, S. Zahendra, and S. Hardy. 2019. Bumble bee (Bombus) distribution and diversity in Vermont, USA: a century of change. Journal of Insect Conservation 23:45-62. https://doi.org/10.1007/s10841-018-0113-5.

Russo, L. 2016. Positive and negative impacts of non-native bee species around the world. Insects 7:69. https://doi.org/10.3390/insects7040069.

Sáez, A., P. Negri, M. Viel, and M. A. Aizen. 2019. Pollination efficiency of artificial and bee pollination practices in kiwifruit. Scientia Horticulturae 246:1017-1021. https://doi.org/10.1016/j.scienta.2018.11.072.

Sáez, A., R. Aguilar, L. Ashworth, G. Gleiser, C. L. Morales, A. Traveset, and M. A. Aizen. 2022. Managed honeybees decrease pollination limitation in self-compatible but not in self-incompatible crops. Proceedings of the Royal Society B: Biological Sciences 289:20220086. https://doi.org/10.1098/rspb.2022.0086.

Senapathi, D., J. Fründ, M. Albrecht, M. P. D. Garratt, D. Kleijn, B. J. Pickles, S. G. Potts, J. An, G. K. S. Andersson, S. Bänsch, P. Basu, F. Benjamin, A. D. M. Bezerra, R. Bhattacharya, J. C. Biesmeijer, B. Blaauw, E. J. Blitzer, C. A. Brittain, L. G. Carvalheiro, D. P. Cariveau, P. Chakraborty, A. Chatterjee, S. Chatterjee, S. Cusser, B. N. Danforth, E. Degani, B. M. Freitas, L. A. Garibaldi, B. Geslin, G. A. De Groot, T. Harrison, B. Howlett, R. Isaacs, S. Jha, B. K. Klatt, K. Krewenka, S. Leigh, S. A. M. Lindström, Y. Mandelik, M. McKerchar, M. Park, G. Pisanty, R. Rader, M. Reemer, M. Rundlöf, B. Smith, H. G. Smith, P. N. Silva, I. Steffan-Dewenter, T. Tscharntke, S. Webber, D. B. Westbury, C. Westphal, J. B. Wickens, V. J. Wickens, R. Winfree, H. Zhang, and A. M. Klein. 2021. Wild insect diversity increases inter-annual stability in global crop pollinator communities. Proceedings of the Royal Society B: Biological Sciences 288:20210212. https://doi.org/10.1098/rspb.2021.0212.

Sharma, M., S. K. Gupta, and A. K. Mondal. 2012. Production and trade of major world oil crops. Pp. 1-15 Technological innovations in major world oil crops. Volume 1. Springer, New York, NY, USA. https://doi.org/10.1007/978-1-4614-0356-2_1.

Smith, M. R., G. M. Singh, D. Mozaffarian, and S. S. Myers. 2015. Effects of decreases of animal pollinators on human nutrition and global health: a modelling analysis. Lancet 386:1964-1972. https://doi.org/10.1016/S0140-6736(15)61085-6.

Somerville, C. 2007. Biofuels. Current Biology 17:R115-9. https://doi.org/10.1016/j.cub.2007.01.010.

Soroye, P., T. Newbold, and J. Kerr. 2020. Climate change contributes to widespread declines among bumble bees across continents. Science 367:685-688. https://doi.org/10.1126/science.aax8591.

Steffan-Dewenter, I. 2003. Seed set of male-sterile and male-fertile oilseed rape (Brassica napus) in relation to pollinator density. Apidologie 34:227-235. https://doi.org/10.1051/apido:2003015.

Stout, J. C., and C. L. Morales. 2009. Ecological impacts of invasive alien species on bees. Apidologie 40:388-409. https://doi.org/10.1051/apido/2009023.

Thomson, D. M. 2016. Local bumble bee decline linked to recovery of honey bees, drought effects on floral resources. Ecology Letters 19:1247-1255. https://doi.org/10.1111/ele.12659.

Turnbull, L. A., M. J. Crawley, and M. Rees. 2000. Are plant populations seed-limited? A review of seed sowing experiments. Oikos 88:225-238. https://doi.org/10.1034/j.1600-0706.2000.880201.x.

Vaissière, B., B. Freitas, and B. Gemmill-Herren. 2011. Protocol to detect and assess pollination deficits in crops: a handbook for its use. FAO, Rome, Italy.

Vanbergen, A. J. A. J., A. Espíndola, and M. A. Aizen. 2018. Risks to pollinators and pollination from invasive alien species. Nature, Ecology and Evolution 2:16-25. https://doi.org/10.1038/s41559-017-0412-3.

Westphal, C., I. Steffan-Dewenter, and T. Tscharntke. 2003. Mass flowering crops enhance pollinator densities at a landscape scale. Ecology Letters 6:961-965. https://doi.org/10.1046/j.1461-0248.2003.00523.x.

Winfree, R., R. Aguilar, D. P. Vázquez, G. LeBuhn, and M. A. Aizen. 2009. A meta-analysis of bees´ responses to anthropogenic disturbance. Ecology 90:2068-2076. https://doi.org/10.1890/08-1245.1.

Winfree, R., J. R. Reilly, I. Bartomeus, D. P. Cariveau, N. M. Williams, and J. Gibbs. 2018. Species turnover promotes the importance of bee diversity for crop pollination at regional scales. Science 359:791-793. https://doi.org/10.1126/SCIENCE.AAO2117.

Winston, M. L. 1987. The biology of the honey bee. Harvard University Press, Cambridge, MA, USA. https://doi.org/10.1007/bf02224064.

Wurz, A., I. Grass, T. Tscharntke. 2021. Hand pollination of global crops-a systematic review. Basic and Applied Ecology 56:299-321. https://doi.org/10.1016/j.baae.2021.08.008.

Zattara, E. E., and M. A. Aizen. 2021. Worldwide occurrence records suggest a global decline in bee species richness. One Earth 4:114-123. https://doi.org/10.1016/j.oneear.2020.12.005.

Myth and reality of a global crisis for agricultural pollination

Descargas

Publicado

2022-05-10

Cómo citar

Aizen, M. A., Garibaldi, L. A., & Harder, L. D. (2022). Mito y realidad de una crisis global de la polinización en la agricultura. Ecología Austral, 32(2), 698–715. https://doi.org/10.25260/EA.22.32.2.1.1875