Spatiotemporal availability of melliferous resources in northwestern Argentine Patagonia
DOI:
https://doi.org/10.25260/EA.23.33.3.0.2180Keywords:
Apis mellifera, nectar, pollen, richness, exotic plant species, sustainable beekeepingAbstract
Beekeeping in northwestern Argentine Patagonia is a small-scale production with great potential for development. Knowledge of the spatial and temporal distribution of the foraging plants that contribute to the nutrition of Apis mellifera hives is essential to plan and support this development. Classification of plant communities into units of melliferous flora can be a helpful tool for beekeeping and landscape management, informing beekeepers where and when the floral resources are available. We review the distribution in plant communities and the flowering time of melliferous species found in north-western Argentine Patagonia. We then characterize the richness and composition of melliferous species in these communities and we identify melliferous flora units and their flowering curves (phenology) based on their similarity. We identified a total of 72 botanical families, 191 genera and 254 melliferous species (114 native and 140 exotic). Melliferous species were distributed across 20 plant communities, with the greatest richness in anthropogenic and arid units. In general, the greatest richness of flowering species occurs between November and January, with a peak of nearly 170 species flowering between December and January. The increased availability of floral resources in anthropogenic areas would suggest that we should promote the development of beekeeping in these areas and restrict the pressure on natural environments. However, the large number of exotic plant species used by Apis mellifera highlights the importance of carefully planning and monitoring beekeeping development, recording the location of apiaries and the number of hives, as well as the potential effects on native pollinators and pollination of melliferous plant species.
References
Agüero, J. I., O. Rollin, J. P. Torretta, M. A. Aizen, F. Requier, et al. 2018. Impactos de la abeja melífera sobre plantas y abejas silvestres en hábitats naturales. Revista Ecosistemas 27(2):60-69. https://doi.org/10.7818/ECOS.1365.
Agüero, J. I., N. Pérez-Méndez, J. P. Torretta, and L. A. Garibaldi. 2020. Impact of invasive bees on plant-pollinator interactions and reproductive success of plant species in mixed Nothofagus Antarctica forests. Neotropical Entomology 49(4):557-567. https://doi.org/10.1007/s13744-020-00787-6.
Aizen, M. A., D. P. Vázquez, and C. Smith-Ramírez. 2002. Historia natural y conservación de los mutualismos planta-animal del bosque templado de Sudamérica austral. Revista Chilena de Historia Natural 75(1):79-97. https://doi.org/10.4067/S0716-078X2002000100008.
Aizen, M. A., C. L. Morales, and J. M. Morales. 2008. Invasive mutualists erode native pollination webs. PLoS Biology 6(2):e31. https://doi.org/10.1371/journal.pbio.0060031.
Aizen, M. A., C. L. Morales, D. P. Vázquez, L. A. Garibaldi, A. Sáez, et al. 2014. When mutualism goes bad: density‐dependent impacts of introduced bees on plant reproduction. New Phytologist 204(2):322-328. https://doi.org/10.1111/nph.12924.
Aloisi, P. V., A. E. Forcone, and M. Amadei. 2013. Contribution to the palynological, physicochemical and organoleptic characterization of Mulinum spinosum (Apiaceae) honeys from Patagonia, Argentina. Interciencia 38(7):528-534.
Andrada, A. 2003. Flora utilizada por Apis mellifera L. en el sur del Caldenal (Provincia Fitogeográfica del Espinal), Argentina. Revista del Museo Argentino de Ciencias Naturales (nueva serie) 5(2):329-336. https://doi.org/10.22179/REVMACN.5.63.
Baquero, M., A. Lucio-Paredes, and R. Vinueza. 2013. Desarrollo Territorial con Enfoque
de Sistemas Agroalimentarios Localizados (AT - SIAL) Valle del Intag, Ecuador.
Beekman, M., and F. L. W. Ratnieks. 2000. Long‐range foraging by the honey‐bee, Apis mellifera L. Functional Ecology 14(4):490-496. https://doi.org/10.1046/j.1365-2435.2000.00443.x.
Bedascarrasbure, E. 2011. Consolidando la apicultura como herramienta de desarrollo. Gestión innovadora: claves del éxito colectivo. Programa Nacional Apícola. Ediciones INTA.
Blüthgen, N., and A. M. Klein. 2011. Functional complementarity and specialisation: the role of biodiversity in plant–pollinator interactions. Basic and Applied Ecology 12(4):282-291. https://doi.org/10.1016/j.baae.2010.11.001.
Bogo, G., G. S. de Groot, S. Medici, J. Winter, M. A. Aizen, et al. 2023. Honeys from Patagonia revealed notable pesticide residues in small-scale agricultural landscapes in the past decade. International Journal of Pest Management 1-9. https://doi.org/10.1080/09670874.2023.2185313.
Brodschneider, R., and K. Crailsheim. 2010. Nutrition and health in honey bees. Apidologie 41(3):278-294. https://doi.org/10.1051/apido/2010012.
Cabrera, A. L. 1971. Fitogeografía de la República Argentina. Boletín De La Sociedad Argentina De Botánica 14:1-2.
Cabrera, M., A. Andrada, and L. Gallez. 2013. Floración de especies con potencial apícola en el Bosque nativo Formoseño, distrito Chaqueño oriental (Argentina). Boletín de la Sociedad Argentina de Botánica 48(3-4):477-491. https://doi.org/10.31055/1851.2372.v48.n3-4.7554.
Couvillon, M. J., F. C. Riddell Pearce, C. Accleton, K. A. Fensome, S. K. Quah, et al. 2015. Honey bee foraging distance depends on month and forage type. Apidologie 46:61-70. https://doi.org/10.1007/s13592-014-0302-5.
Danner, N., A. M. Molitor, S. Schiele, S. Härtel, and I. Steffan‐Dewenter. 2016. Season and landscape composition affect pollen foraging distances and habitat use of honey bees. Ecological Applications 26(6):1920-1929. https://doi.org/10.1890/15-1840.1.
de Groot, G. S., M. A. Aizen, A. Sáez, and C. L. Morales. 2021. Large-scale monoculture reduces honey yield: The case of soybean expansion in Argentina. Agriculture, Ecosystems and Environment 306:107203. https://doi.org/10.1016/j.agee.2020.107203.
de Groot, G. S., S. Svampa, M. A. Aizen, R. Schmucki, and C. I. Morales. 2023: Flora melífera de la Región Andino-Norpatagónica argentina. Consejo Nacional de Investigaciones Científicas y Técnicas. (dataset). URL: hdl.handle.net/11336/183231.
Debnam, S., A. Sáez, M. A. Aizen, and R. M. Callaway. 2021. Exotic insect pollinators and native pollination systems. Plant Ecology 222(9):1075-1088. https://doi.org/10.1007/s11258-021-01162-0.
Doeke, M. A., M. Frazier, and C. M. Grozinger. 2015. Overwintering honey bees: biology and management. Current Opinion in Insect Science 10:185-193. https://doi.org/10.1016/j.cois.2015.05.014.
Ezcurra, C., and C. Brion. 2005. Plantas del Nahuel Huapi: Catálogo de la Flora Vascular del Parque Nacional Nahuel Huapi, Argentina. Universidad Nacional del Comahue; Red Latinoamericana de Botánica. URL: hdl.handle.net/11336/134495.
Ezcurra, C., A. Premoli, C. Souto, M. A. Aizen, M. Arbetman, et al. 2014. La vegetación de la Región Andino-Norpatagónica tiene su Historia en E. Raffaele, M. de Torres Curth, C. L. Morales and T. Kirtberger (eds.). Ecología E Historia Natural De La Patagonia Andina: Un Cuarto De Siglo De Investigación En Biogeografía, Ecología y Conservación. 1a edición. Ciudad Autónoma de Buenos Aires: Fundación de Historia Natural Félix de Azara.
FAOSTAT. 2022. Food and Agriculture Organization Corporate Statistical Database.
URL: fao.org/faostat/en.
Fagundez, G. A., P. D. Reinoso, and P. G. Aceñolaza. 2016. Caracterización y fenología de especies de interés apícola en el departamento Diamante (Entre Ríos, Argentina). Boletín de la Sociedad Argentina de Botánica 51(2):243-267. https://doi.org/10.31055/1851.2372.v51.n2.14837.
Filipiak, M., K. Kuszewska, M. Asselman, B. Denisow, E. Stawiarz, et al. 2017. Ecological stoichiometry of the honeybee: Pollen diversity and adequate species composition are needed to mitigate limitations imposed on the growth and development of bees by pollen quality. PLoS ONE 12(8):e0183236. https://doi.org/10.1371/journal.pone.0183236.
Filipiak, M., A. Walczyńska, B. Denisow, T. Petanidou, and E. Ziółkowska. 2022. Phenology and production of pollen, nectar, and sugar in 1612 plant species from various environments. Ecology 103(7):e3705. https://doi.org/10.1002/ecy.3705.
Flora Argentina. 2022. Instituto de Botánica Darwinion (CONICET). URL: floraargentina.edu.ar.
Forcone, A., O. Bravo, and M. G. Ayestarán. 2003. Intraannual variations in the pollinic spectrum of honey from the lower valley of the River Chubut (Patagonia, Argentina). Spanish Journal of Agricultural Research 1(2):29-36. https://doi.org/10.5424/sjar/2003012-18.
Forcone, A., G. Ayestarán, A. Kutschker, and J. García. 2005. Palynological characterization of honeys from the Andean Patagonia (Chubut, Argentina). Grana 44(3):202-208. https://doi.org/10.1080/00173130500205816.
Forcone, A., and A. Kutschker. 2006. Floración de las especies de interés apícola en el noroeste de Chubut, Argentina. Revista del Museo Argentino de Ciencias Naturales (nueva serie) 8(2):151-157. https://doi.org/10.22179/REVMACN.8.314.
Forcone, A. 2008. Pollen analysis of honey from Chubut (Argentinean Patagonia). Grana 47(2):147-158. https://doi.org/10.1080/10652460802106340.
Forcone, A., and M. Muñoz. 2009. Palynological and physico‐chemical characterisation of honeys from the north‐west of Santa Cruz (Argentinean Patagonia). Grana 48(1):67-76. https://doi.org/10.1080/00173130802602033.
Forcone, A., A. Calderón, and A. Kutschker. 2013. Apicultural pollen from the Andean region of Chubut (Argentinean Patagonia). Grana 52(1):49-58. https://doi.org/10.1080/00173134.2012.717964.
Gómez Riera, P., I. Bruzone, and D. S. Kirschbaum. 2014. Visión prospectiva de la cadena de frutas finas al 2030. Buenos Aires: Ministerio de Ciencia, Tecnología e Innovación Productiva.
Gurini, L. B., and A. Basilio. 1995. Flora apícola en el Delta del Paraná. Darwiniana 337-346.
Harbo, J. R. 1986. Effect of population size on brood production, worker survival and honey gain in colonies of honeybees. Journal of Apicultural Research 25(1):22-29. https://doi.org/10.1080/00218839.1986.11100687.
Hijmans, R. J., S. E. Cameron, J. L. Parra, P. G. Jones, and A. Jarvis. 2005. Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology: A Journal of the Royal Meteorological Society 25(15):1965-1978. https://doi.org/10.1002/joc.1276.
Huang, Z. 2010. Honey bee nutrition. American Bee Journal 150(8):773-776.
Jobbágy, E. G., J. M. Paruelo, and R. J. León. 1996. Vegetation heterogeneity and diversity in flat and mountain landscapes of Patagonia (Argentina). Journal of vegetation Science 7(4):599-608. https://doi.org/10.2307/3236310.
Kahle, D., and H. Wickham. 2013. ggmap: Spatial Visualization with ggplot2. The R Journal 5(1):144-161. https://doi.org/10.32614/RJ-2013-014.
Kitzberger, T. 2012. Ecotones as complex arenas of disturbance, climate, and human impacts: the trans-Andean forest-steppe ecotone of northern Patagonia. Pp. 59-88 en Ecotones Between Forest and Grassland. Springer, New York, NY. https://doi.org/10.1007/978-1-4614-3797-0_3.
MAGyP. 2022. Mapa de identidad de mieles. Ministerio de Agricultura, Ganadería y Pesca (MAGyP). URL: magyp.gob.ar/apicultura/mapa.php.
Maharramov, J., I. Meeus, K. Maebe, M. Arbetman, C. Morales, et al. 2013. Genetic variability of the neogregarine Apicystis bombi, an etiological agent of an emergent bumblebee disease. PLoS ONE 8(12):e81475. https://doi.org/10.1371/journal.pone.0081475.
Massaccesi, C. A. 2002. Manual de Apicultura en la Patagonia Andina. Instituto Nacional de Tecnología Agropecuaria (INTA).
Morales, C. L., and M. A. Aizen. 2002. Does invasion of exotic plants promote invasion of exotic flower visitors? A case study from the temperate forests of the southern Andes. Biological Invasions 4(1):87-100. https://doi.org/10.1023/A:1020513012689.
Naab, O. A., M. A. Caccavari, H. Troaini, and A. Ponce. 2001. Melisopalinología y su relación con la vegetación en el Departamento de Utracán, La Pampa, Argentina. URL: hdl.handle.net/10396/11263.
Naab, O., and M. A. Tamame. 2007. Flora apícola primaveral en la región del Monte de la Provincia de La Pampa (Argentina). Boletín de la Sociedad Argentina de Botánica 42(3-4):251-259.
Nicolson, S. W. 2011. Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. African Zoology 46(2):197-204. https://doi.org/10.1080/15627020.2011.11407495.
Ogilvie, J. E., and J. R. Forrest. 2017. Interactions between bee foraging and floral resource phenology shape bee populations and communities. Current Opinion in Insect Science 21:75-82. https://doi.org/10.1016/j.cois.2017.05.015.
Oksanen, J., G. Simpson, F. Blanchet, R. Kindt, P. Legendre, et al. 2022. _vegan: Community Ecology Package_. R package version 2.6-2. URL: CRAN.R-project.org/package=vegan.
Patrignani, M., G. A. Fagúndez, C. Tananaki, A. Thrasyvoulou, and C. E. Lupano. 2018. Volatile compounds of Argentinean honeys: Correlation with floral and geographical origin. Food Chemistry 246:32-40. https://doi.org/10.1016/j.foodchem.2017.11.010.
Peri, P. L., L. E. Tejera, I. L. Amico, A. Von Müller, G. J. Martínez Pastur, et al. 2016. Estado de situación del sector forestal en Patagonia Sur. Centro Regional Patagonia Sur. Informe técnico. Instituto Nacional de Tecnología Agropecuaria (INTA), Argentina.
Pietrantuono, A. L., F. Requier, V. Fernández-Arhex, J. Winter, G. Huerta, et al. 2019. Honeybees generalize among pollen scents from plants flowering in the same seasonal period. Journal of Experimental Biology 222(21):jeb201335. https://doi.org/10.1242/jeb.201335.
POWO. 2022. Plants of the World Online. Facilitated by the Royal Botanic Gardens, Kew. URL: plantsoftheworldonline.org.
Queimaliños, C., M. Reissig, G. L. Pérez, C. S. Cárdenas, M. Gerea, et al. 2019. Linking landscape heterogeneity with lake dissolved organic matter properties assessed through absorbance and fluorescence spectroscopy: Spatial and seasonal patterns in temperate lakes of Southern Andes (Patagonia, Argentina). Science of the Total Environment 686:223-235. https://doi.org/10.1016/j.scitotenv.2019.05.396.
R Core Team. 2022. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL: R-project.org.
RENAPA. 2022. Registro Nacional de Productores Apícolas. Ministerio de Agricultura, Ganadería y Pesca (MAGyP). URL: tinyurl.com/58x65uhk.
Reserva de Biósfera Andino-Norpatagónica. URL: tinyurl.com/yfjtpdj6.
Requier, F., J. F. Odoux, M. Henry, and V. Bretagnolle. 2017. The carry‐over effects of pollen shortage decrease the survival of honeybee colonies in farmlands. Journal of Applied Ecology 54(4):1161-1170. https://doi.org/10.1111/1365-2664.12836.
Roulston, T. A. H., J. H. Cane, and S. L. Buchmann. 2000. What governs protein content of pollen: pollinator preferences, pollen–pistil interactions, or phylogeny? Ecological Monographs 70(4):617-643. https://doi.org/10.1890/0012-9615(2000)070[0617:WGPCOP]2.0.CO;2.
Salgado, C. R., G. Pieszko, and M. C. Tellería. 2014. Aporte de la Melisopalinología al conocimiento de la flora melífera de un sector de la Provincia Fitogeográfica Chaqueña, Argentina. Boletín de la Sociedad Argentina de Botánica 49(4):513-524. https://doi.org/10.31055/1851.2372.v49.n4.9889.
Schmidt, J. O., S. C. Thoenes, and M. D. Levin. 1987. Survival of honey bees, Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Annals of the Entomological Society of America 80(2):176-183. https://doi.org/10.1093/aesa/80.2.176.
Seeley, T. D., and P. K. Visscher. 1985. Survival of honeybees in cold climates: the critical timing of colony growth and reproduction. Ecological Entomology 10(1):81-88. https://doi.org/10.1111/j.1365-2311.1985.tb00537.x.
Steffan-Dewenter, I., and A. Kuhn. 2003. Honeybee foraging in differentially structured landscapes. Proceedings of the Royal Society of London. Series B: Biological Sciences 270(1515):569-575. https://doi.org/10.1098/rspb.2002.2292.
Tellería, M. C. 1995. Plantas de importancia apícola del Distrito Oriental de la Región Pampeana (Argentina). Bol Soc Argent Bot 30(3-4):131-136.
UNESCO 2020. URL: en.unesco.org/biosphere/lac/andino-norpatagonica.
UNESCO 2022. URL: en.unesco.org/biosphere/about.
Winston, M. L.1991. The Biology of the Honey Bee. Harvard University Press.
Downloads
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Grecia S. de Groot, Suyai Svampa, Marcelo A. Aizen, Reto Schmucki, Carolina L. Morales
This work is licensed under a Creative Commons Attribution 3.0 Unported License.
Authors retain their rights as follows: 1) by granting the journal the right to its first publication, and 2) by registering the published article with a Creative Commons Attribution License (CC-BY 4.0), which allows authors and third parties to view and use it as long as they clearly mention its origin (citation or reference, including authorship and first publication in this journal). Authors can make other non-exclusive distribution agreements as long as they clearly indicate their origin and are encouraged to widely share and disseminate the published version of their work.
