Estimación del servicio de polinización en un cultivo de alfalfa (Medicago sativa L.) mediante la cuantificación de flores disparadas

Joana P. Haedo; Sofía Graffigna; Lucía C. Martínez; Juan P. Torretta; Hugo J. Marrero

doi:10.25260/EA.22.32.2.0.1770

Authors

Joana P. Haedo Centro de Recursos Naturales Renovables de la Zona Semiárida (CERZOS), CONICET. Laboratorio de Interacciones Bióticas en Agroecosistemas (LIBA). Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina (CONICET)
Sofía Graffigna Centro de Recursos Naturales Renovables de la Zona Semiárida (CERZOS), CONICET. Laboratorio de Interacciones Bióticas en Agroecosistemas (LIBA). Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina (CONICET)
Lucía C. Martínez Laboratorio de Interacciones Bióticas en Agroecosistemas (LIBA). Departamento de Biología, Bioquímica y Farmacia, Universidad Nacional del Sur. Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina (CONICET)
Juan P. Torretta Cátedra de Botánica General, Facultad de Agronomía, Universidad de Buenos Aires. Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina (CONICET)
Hugo J. Marrero Centro de Recursos Naturales Renovables de la Zona Semiárida (CERZOS), CONICET. Laboratorio de Interacciones Bióticas en Agroecosistemas (LIBA). Consejo Nacional de Investigaciones Científicas y Técnicas de Argentina (CONICET)

DOI:

https://doi.org/10.25260/EA.22.32.2.0.1770

Keywords:

biotic pollination, crops, Medicago sativa, fruit set

Abstract

Biotic pollination directly affects yield of most of crop species. Therefore, monitoring the pollination service in a crop field is very important, although it rarely occurs. Certain pollination mechanisms, such as the explosive mechanism of flowers, would allow farmers to estimate the crop yield quickly and efficiently. The objective of this study is to evaluate a methodology for estimating the pollination service in crops with explosive pollination mechanism through the quantification of tripped flowers. For this, we used 16 alfalfa (Medicago sativa) lots in eight fields located in the Valle Bonaerense del Río Colorado, where we conducted pollination experiments and assessed the proportion of tripped flowers (visited) per inflorescence and the plant reproductive success (estimated as fruit set). Our results showed that a) in alfalfa, non-tripped flowers have a very low probability of becoming fruit, b) a single effective visit is sufficient for fructification, and c) successive visits do not increment the probability of fruit formation. On the other hand, we demonstrated that the proportion of tripped flowers is positively related to fruit set. Our results evidence that the assessment of tripped flowers can be an efficient tool to quantify the pollination service in a crop with an explosive mechanism. Although this methodology does not explain the causes of fructification deficiency, this tool may become the first step in crop problems detection, without neglecting the long-term studies that will improve pollination service in an effective way.

References

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. 2019. Global agricultural productivity is threatened by increasing pollinator dependence without a parallel increase in crop diversification. Global Change Biology 25(10):3516-3527. https://doi.org/10.1111/gcb.14736.

Alemán, M., T. Figueroa-Fleming, A. Etcheverry, S. Sühring, and P. Ortega-Baes. 2014. The explosive pollination mechanism in Papilionoideae (Leguminosae): an analysis with three Desmodium species. Plant Systematics and Evolution 300(1):177-186. https://doi.org/10.1007/s00606-013-0869-8.

Aluri, R. J., and C. Subba Reddi. 1995. Explosive pollen release and pollination in flowering plants. Proceedings - Indian National Science Academy Part B 61:323-323.

Arroyo, M. T. K. 1981. Breeding systems and pollination biology in Leguminosae. Pp. 723-769 en R. M. Polhill and P. H. Raven (eds.). Advances in legume systematics, part 2. The Royal Botanical Gardens, Kew, London, United Kingdom.

Batra, S. W. T. 1976. Comparative efficiency of alfalfa pollination by Nomia melanderi, Megachile rotundata, Anthidium florentinum and Pithitis smaragdula (Hymenoptera: Apoidea). J Kans Entomol Soc 49:18-22.

Breeze, T. D., A. P. Bailey, K. G. Balcombe, and S.G. Potts. 2011. Pollination services in the UK: How important are honeybees? Agriculture, Ecosystems and Environment 142(3-4):137-143. https://doi.org/10.1016/j.agee.2011.03.020.

Brittain, C., R. Bommarco, M. Vighi, S. Barmaz, J. Settele, and S. G. Potts. 2010. The impact of an insecticide on insect flower visitation and pollination in an agricultural landscape. Agricultural and Forest Entomology 12(3):259-266. https://doi.org/10.1111/j.1461-9563.2010.00485.x.

Bohart, G. E. 1957. Pollination of alfalfa and red clover. Annual Review of Entomology 2(1):355-380. https://doi.org/10.1146/annurev.en.02.010157.002035.

Bohart, G. E. 1958. Alfalfa pollinators with special reference to species other than honey bees. Proc 10th Internatl Congr 4:929-937.

Boreux, V., C. G. Kushalappa, P. Vaast, and J. Ghazoul. 2013. Interactive effects among ecosystem services and management practices on crop production: pollination in coffee agroforestry systems. Proceedings of the National Academy of Sciences 110(21):8387-8392. https://doi.org/10.1073/pnas.1210590110.

Bos, M. M., I. Steffan-Dewenter, and T. Tscharntke. 2007. Shade tree management affects fruit abortion, insect pests and pathogens of cacao. Agriculture, Ecosystems and Environment 120:201-205. https://doi.org/10.1016/j.agee.2006.09.004.

Cane, J. H. 2002. Pollinating bees (Hymenoptera: Apiformes) of U.S. alfalfa compared for rates of pod and seed set. J Econ Entomol 95:22-27. https://doi.org/10.1603/0022-0493-95.1.22.

Chen, M., and X. A. Zuo. 2018. Pollen limitation and resource limitation affect the reproductive success of Medicago sativa L. BMC Ecology 18(1):28. https://doi.org/10.1186/s12898-018-0184-x.

Dainese, M., E. A. Martin, M. A. Aizen, M. Albrecht, I. Bartomeus, et al. 2019. A global synthesis reveals biodiversity-mediated benefits for crop production. Science Advances 5(10):eaax012. https://doi.org/10.1126/sciadv.aax0121.

Figueroa-Fleming, T., and F. T. Etcheverry. 2017. Comparing the efficiency of pollination mechanisms in Papilionoideae. Arthropod-Plant Interactions 11:273-283. https://doi.org/10.1007/s11829-017-9515-7.

Fung, H. F., and J. D. Thomson. 2017. Does lack of pollination extend flower life? Journal of Pollination Ecology 21:86-91. https://doi.org/10.26786/1920-7603(2017)447.

Fürst, M. A., D. P. McMahon, J. L. Osborne, R. J. Paxton, and M. Brown. 2014. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506(7488):364-366. https://doi.org/10.1038/nature12977.

Gallai, N., J. 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.

Galloni, M., and G. Cristofolini. 2003. Floral rewards and pollination in Cytiseae (Fabaceae). Plant Systematics and Evolution 238(1):127-137. https://doi.org/10.1007/s00606-002-0270-5.

Garibaldi, L. A., I. Steffan-Dewenter, R. Winfree, M. A. Aizen, R. Bommarco, et al. 2013. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339(6127): 1608-1611. https://doi.org/10.1126/science.1230200.

Garibaldi, L. A., L. G. Carvalheiro, S. D. Leonhardt, M. A. Aizen, and B. R. Blaauw. 2014. From research to action: enhancing crop yield through wild pollinators. Frontiers in Ecology and the Environment 12(8):439-447. https://doi.org/10.1890/130330.

Garibaldi, L. A., A. Sáez, M. A. Aizen, T. Fijen, and I. Bartomeus. 2020. Crop pollination management needs flower‐visitor monitoring and target values. Journal of Applied Ecology 57(4):664-670. https://doi.org/10.1111/1365-2664.13574.

Gavini, S. S., and A. Farji-Brener. 2015. La importancia del color: morfos florales, tasas de visita y éxito reproductivo en el arbusto Sarothamnus scoparius. Ecología Austral 25:204-211. https://doi.org/10.25260/EA.15.25.3.0.82.

Goulson, D. 2003. Effects of introduced bees on native ecosystems. Annual Review of Ecology, Evolution, and Systematics 34(1):1-26. https://doi.org/10.1146/annurev.ecolsys.34.011802.132355.

Goulson, D. 2010. Impacts of non-native bumblebees in Western Europe and North America. Applied Entomology and Zoology 45(1):7-12. https://doi.org/10.1303/aez.2010.7.

Graffigna, S., H. J. Marrero, and J. P. Torretta. 2021. Glyphosate commercial formulation negatively affects the reproductive success of solitary wild bees in a Pampean agroecosystem. Apidologie 52(1):272-281. https://doi.org/10.1007/s13592-020-00816-8.

Groeneveld, J. H., T. Tscharntke, G. Moser, and Y. Clough. 2010. Experimental evidence for stronger cacao yield limitation by pollination than by plant resources. Perspectives in Plant Ecology, Evolution and Systematics 12:183-191. https://doi.org/10.1016/j.ppees.2010.02.005.

Haedo, J. P., L. C. Martínez, S. Graffigna, H. J. Marrero, and J. P. Torretta. 2022. Managed and wild bees contribute to alfalfa (Medicago sativa) pollination. Agriculture, Ecosystems and Environment 324:107711. https://doi.org/10.1016/j.agee.2021.107711.

Hass, A. L., U. G. Kormann, T. Tscharntke, Y. Clough, A. Bosem Baillod, C. Sirami, L. Fahrig, J.-L. Martin, J. Baudry, C. Bertrand, J. Bosch, L. Brotons, F. Burel, R. Georges, D. Giralt, M. Á. Marcos-García, A. Ricarte, G. Siriwardena, and P. Batáry. 2018. Landscape configurational heterogeneity by small-scale agriculture, not crop diversity, maintains pollinators and plant reproduction in western Europe. Proceedings of the Royal Society B: Biological Sciences 285(1872): 20172242. https://doi.org/10.1098/rspb.2017.2242.

Kennedy, C. M., E. Lonsdorf, M. C. Neel, N. M. Williams, T. H. Ricketts, R. Winfree, R. Bommarco, C. Brittain, A. L. Burley, D. Cariveau, L. G. Carvalheiro, N. P. Chacoff, S. A. Cunningham, B. N. Danforth, J.-H. Dudenhöffer, E. Elle, H. R. Gaines, L. A. Garibaldi, C. Gratton, A. Holzschuh, R. Isaacs, S. K. Javorek, S. Jha, A. M. Klein, K. Krewenka, Y. Mandelik, M. M. Mayfield, L. Morandin, L. A. Neame, M. Otieno, M. Park, S. G. Potts, M. Rundlöf, A. Saez, I. Steffan-Dewenter, H. Taki, B. Felipe Viana, C. Westphal, J. K. Wilson, S. S. Greenleaf, and C. Kremen. 2013. A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecology Letters 16(5):584-599. https://doi.org/10.1111/ele.12082.

Klein, A. M., B. E. Vaissiere, 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.

Lautenbach, S., R. Seppelt, J. Liebscher, and C. F. Dormann. 2012. Spatial and temporal trends of global pollination benefit. PLoS ONE 7(4):e35954. https://doi.org/10.1371/journal.pone.0035954.

Lázaro, A., and D. Alomar. 2019. Landscape heterogeneity increases the spatial stability of pollination services to almond trees through the stability of pollinator visits. Agriculture, Ecosystems and Environment 279:149-155. https://doi.org/10.1016/j.agee.2019.02.009.

Linsley, G. E. 1946. Insect pollinators of alfalfa in California. J Econ Entomol 39:18-29. https://doi.org/10.1093/jee/39.1.18.

Liss, K. N., M. G. Mitchell, G. K. MacDonald, S. L. Mahajan, J. Méthot, A. L. Jacob, D. Y. Maguire, G. S. Metson, C. Ziter, K. Dancose, K. Martins, M. Terrado, and E. M. Bennett. 2013. Variability in ecosystem service measurement: a pollination service case study. Frontiers in Ecology and the Environment 11:414-422. https://doi.org/10.1890/120189.

López, J., T. Rodríguez-Riaño, A. Ortega-Olivencia, J. A. Devesa, and T. Ruiz. 1999. Pollination mechanisms and pollen-ovule ratios in some Genisteae (Fabaceae) from Southwestern Europe. Plant Systematics and Evolution 216:23-47. https://doi.org/10.1007/BF00985099.

Melathopoulos, A. P., G. C. Cutler, and P. Tyedmers. 2015. Where is the value in valuing pollination ecosystem services to agriculture? Ecological Economics 109:59-70. https://doi.org/10.1016/j.ecolecon.2014.11.007.

Morales, C. L., A. Sáez, M. P. Arbetman, L. Cavallero, and M. A. Aizen. 2014. Detrimental effects of volcanic ash deposition on bee fauna and plant-pollinator interactions. Ecología Austral 24:42-50. https://doi.org/10.25260/EA.14.24.1.0.36.

Morris, W. F., D. P. Vázquez, and N. P. Chacoff. 2010. Benefit and cost curves for typical pollination mutualisms. Ecology 91:1276-1285. https://doi.org/10.1890/08-2278.1.

Moschetti, C. J., E. M. Martinez, E. M. Echeverría, and L. M. Ávalos. 2007. Producción de semilla de alfalfa. Pp. 407-442 en D. H. Basigalup (ed.). El cultivo de alfalfa en Argentina. Ediciones INTA, Buenos Aires, Argentina.

Parker, I. M. 1997. Pollinator limitation of Cytisus scoparius (Scotch broom), an invasive exotic shrub. Ecology 78(5):1457-1470. https://doi.org/10.1890/0012-9658(1997)078[1457:PLOCSS]2.0.CO;2.

Pitts-Singer, T. L., and J. H. Cane. 2011. The alfalfa leafcutting bee, Megachile rotundata: the world’s most intensively managed solitary bee. Annual Review of Entomology 56:221-237. https://doi.org/10.1146/annurev-ento-120709-144836.

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

Rodríguez, N., and M. C. Spada. 2007. Morfología de la alfalfa. Pp. 29-43 en D. H. Basigalup (ed.). El cultivo de alfalfa en Argentina. Ediciones INTA, Buenos Aires, Argentina.

Santa‐Martínez, E., C. Cardoso Castro, A. Flick, M. Sullivan, H. Riday, M. K. Clayton, and J. Brunet. 2021. Bee species visiting Medicago sativa differ in pollen deposition curves with consequences for gene flow. American Journal of Botany 108:1016-1028. https://doi.org/10.1002/ajb2.1683.

Shorthouse, D. P. 2010. SimpleMappr, an online tool to produce publication-quality point maps. URL: simplemappr.net.

Stanley, D. A., M. P. Garratt, J. B. Wickens, V. J. Wickens, S. G. Potts, and N. E. Raine. 2015. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528(7583):548. https://doi.org/10.1038/nature16167.

Suzuki, N. 2003. Significance of flower exploding pollination on the reproduction of the Scotch broom, Cytisus scoparius (Leguminosae). Ecological Research 18(5):523-532. https://doi.org/10.1046/j.1440-1703.2003.00575.x.

Tasei, J. N., M. Picard, and S. Carre. 1978. Les insectes pollinisateurs de la luzerne (Medicago sativa L.) en France. Apidologie 9:175-194. https://doi.org/10.1051/apido:19780302.

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

Viands, D. R., P. Sun, and D. K. Barnes. 1988. Pollination control: Mechanical and sterility. Pp. 931-960 en A. A. Hanson, D. K. Barnes and R. R. Hill Jr. (eds.). Alfalfa and Alfalfa Improvement. American Society of Agronomy, Inc. Publishers, Madison, Wisconsin, USA. https://doi.org/10.2134/agronmonogr29.c30.

Wang, X., H. Liu, L. Huang, S. Zhang, Z. Deng, J. Li, and L. Jin. 2012. Biodiversity of wild alfalfa pollinators and their temporal foraging characters in Hexi Corridor, Northwest China. Entomol Fennica 23:4-12. https://doi.org/10.33338/ef.84561.

Watmough, R. H. 1999. The potential of Megachile gratiosa Cameron, Xylocopa caffra (Linnaeus) (Hymenoptera: Megachilidae and Anthophoridae) and other solitary bees as pollinators of alfalfa, Medicago sativa L. (Fabaceae), in the Oudtshoorn District, South Africa. Afr Entomol 7:312-315. URL: journals.co.za/doi/pdf/10.10520/AJA10213589_376.