Estudio de monitoreo de campo para explorar la exposición de la abeja melífera a residuos de pesticidas en huertos frutales
Resumen
Objetivo del estudio: La abeja melífera (Apis mellifera L.) está amenazada debido a diversas presiones; entre ellas, la fragmentación de su hábitat, las plagas o enfermedades que la afectan y al mal uso de productos fitosanitarios (PF). Este trabajo tuvo como objetivo evaluar y comparar el grado de exposición de A. mellifera a residuos de PF en huertos frutales, tanto en producción convencional como ecológica.
Área de estudio: Región de Murcia (España).
Material y métodos: Durante un período de tres años, se organizaron campañas de monitoreo de campo en huertos de melocotonero y albaricoquero, tanto bajo manejo convencional como ecológico, coincidiendo con el período de floración. La evaluación de la exposición se basó en la caracterización química de residuos de pesticidas mediante una detección no dirigida con espectrometría de alta resolución de masa exacta (HRAM).
Resultados principales: Los hallazgos de este estudio revelan que se detectaron residuos de pesticidas en abejas melíferas capturadas tanto en huertos convencionales como ecológicos. Los residuos de pesticidas identificados de forma tentativa fueron carbetamida, flufenacet, iprovalicarbo, isoprocarb y espiromesifeno. Dado que las abejas melíferas, particularmente las recolectoras, vuelan hasta varios km de distancia desde la colmena para recolectar polen y néctar, éstas podrían visitar parcelas manejadas convencionalmente donde los cultivos se tratan con PF.
Aspectos destacados de la investigación: Este estudio evidencia que, en huertos frutales, las abejas recolectoras están expuestas a agroquímicos durante su actividad de forrajeo en las flores de los árboles frutales tratados, ya sean de parcelas contiguas o distantes. La exposición de las abejas a residuos de pesticidas en huertos orgánicos puede deberse a la alta persistencia de algunas de estas sustancias en el medio ambiente o a la proximidad de otros huertos donde se aplican PF.
Descargas
Citas
Abrol DP, 2015. Pollination biology, Vol. 1: Pests and pollinators of fruit crops. Springer Cham, Switzerland. 452 pp. https://doi.org/10.1007/978-3-319-21085-8
Amaya-Márquez M, 2009. Floral constancy in bees: a revision of theories and a comparison with other pollinators. Rev Colomb Entomol 35(2), 206-216. https://doi.org/10.25100/socolen.v35i2.9221
Beekman M, Ratnieks FLW, 2000. Long‐range foraging by the honey‐bee, Apis mellifera L. Funct Ecol 14, 490-496. https://doi.org/10.1046/j.1365-2435.2000.00443.x
Bielza P, Contreras J, Quinto V, Izquierdo J, Mansanet V, Elbert A, 2005. Effects of Oberon® 240 SC on bumblebees pollinating greenhouse tomatoes. Pflanzenschutz-Nachrichten Bayer 58(3), 469-484.
Böhme F, Bischoff G, Zebitz CPW, Rosenkranz P, Wallner K, 2018. Pesticide residue survey of pollen loads collected by honeybees (Apis mellifera) in daily intervals at three agricultural sites in South Germany. PLoS ONE 13(7): e0199995. https://doi.org/10.1371/journal.pone.0199995
Brunet J, Fragoso FP, 2024. What are the main reasons for the worldwide decline in pollinator populations? CABI Reviews 19:1. https://doi.org/10.1079/cabireviews.2024.0016
Calatayud-Vernich P, Calatayud F, Simó E, Suarez-Varela MM, Picó Y, 2016. Influence of pesticide use in fruit orchards during blooming on honeybee mortality in 4 experimental apiaries. Sci Total Environ 541, 33-41. http://dx.doi.org/10.1016/j.scitotenv.2015.08.131
Choudhary A, Sharma DC, 2008. Dynamics of pesticide residues in nectar and pollen of mustard (Brassica juncea (L.) Czern.) grown in Himachal Pradesh (India). Environ Monit Assess 144, 143–150. https://doi.org/10.1007/s10661-007-9952-3
Di Noi A, Casini S, Campani T, Cai G, Caliani I, 2021. Review on sublethal effects of environmental contaminants in honey bees (Apis mellifera), knowledge gaps and future perspectives. Int J Environ Res Public Health 18, 1863. https://doi.org/10.3390/ijerph18041863
EC, 2013a. Commission Regulation (EU) No 283/2013 of 1 March 2013 setting out the data requirements for active substances, in accordance with Regulation (EC) No 1107/2009 of the European Parliament and of the Council concerning the placing of plant protection products on the market. 21/11/2022. https://eur-lex.europa.eu/eli/reg/2013/283/2022-11-21
EC, 2013b. Commission Regulation (EU) No 284/2013 of 1 March 2013 setting out the data requirements for plant protection products, in accordance with Regulation (EC) No 1107/2009 of the European Parliament and of the Council concerning the placing of plant protection products on the market. 21/11/2022. https://eur-lex.europa.eu/eli/reg/2013/284/2022-11-21
EC, 2017. Guidance document on analytical quality control and method validation procedures for pesticide residues and analysis in food and feed. SANTE/11813/2017. https://eurl-pesticides.eu/userfiles/file/EurlALL/SANTE_11813_2017-fin.pdf
EC, 2024. EU Pesticides Database (v3.2). https://food.ec.europa.eu/plants/pesticides/eu-pesticides-database_en [22 April 2024].
EFSA, 2012. Conclusion on the peer review of the pesticide risk assessment of the active substance spiromesifen. EFSA J 2012, 10(10):2879, 56 pp. https://doi.org/10.2903/j.efsa.2012.2879
EFSA, 2015. Conclusion on the peer review of the pesticide risk assessment of the active substance iprovalicarb. EFSA J 2015, 13(4):4060, 82 pp. https://doi.org/10.2903/j.efsa.2015.4060
EFSA, Adriaanse P, Arce A, Focks A, Ingels B, Jölli D, Lambin S, Rundlöf M, Süßenbach D, Del Aguila M, et al., 2023. Revised guidance on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J 2023, 21(5):7989, 133 pp. https://doi.org/10.2903/j.efsa.2023.7989
EFSA-AR, 2010. Additional report to the DAR on the active substance carbetamide prepared by the Rapporteur Member State (RMS) France in the framework of the Commission Regulation (EC) No 33/2008. https://www.efsa.europa.eu/en/consultations/call/public-consultation-active-substance-carbetamide-additional-report
EFSA-DRAR, 2017. Draft renewal assessment report on the active substance flufenacet prepared by the Rapporteur Member State (RMS) Poland and the co-rapporteur Member State France in the framework of the Commission Regulation (EU) No 1107/2009. https://www.efsa.europa.eu/en/consultations/call/170920
FAO-CGRFA, 2018. Global survey of honeybees and other pollinators. Intergovernmental technical working group on animal genetic resources for food and agriculture. Rome. https://openknowledge.fao.org/server/api/core/bitstreams/99564232-50da-4e25-9baa-0dce7da67936/content
FDA-FVM, 2015. Acceptance criteria for confirmation of identity of chemical residues using exact mass data within the office of foods and veterinary medicine. https://www.fda.gov/media/96499/download
Gray A, Brodschneider R, Adjlane N, Ballis A, Brusbardis V, Charrière J-D, Chlebo R, Coffey MF, Cornelissen B, da Costa CA, et al., 2019. Loss rates of honey bee colonies during winter 2017/18 in 36 countries participating in the COLOSS survey, including effects of forage sources. J Apic Res 58(4), 479-485. https://doi.org/10.1080/00218839.2019.1615661
Gurpegui M, Ornosa C, Sánchez-Ramos I, Cobo A, González-Núñez M, 2017. Abundancia y diversidad de abejas y otros apoideos polinizadores en cultivos de melocotonero y albaricoquero en la región de Murcia en función del manejo fitosanitario. X Congreso Nacional de Entomología Aplicada - XVI Jornadas Científicas de la SEEA, Logroño (Spain), Oct 16-20. pp: 60.
Hung K-LJ, Kingston JM, Albrecht M, Holway DA, Kohn JR, 2018. The worldwide importance of honey bees as pollinators in natural habitats. Proc R Soc B 285: 20172140. https://doi.org/10.1098/rspb.2017.2140
Kim BM, El-Aty AMA, Hwang TE, Jin LT, Kim YS, Shim JH, 2007. Development of an acetylcholinesterase-based detection kit for the determination of organophosphorus and carbamate pesticide residues in agricultural samples. Bull Korean Chem Soc 28(6), 929-935. https://doi.org/10.5012/bkcs.2007.28.6.929
Kral K, Schneider L, 1981. Fine structural localisation of acetylcholinesterase activity in the compound eye of the honeybee (Apis mellifica L.). Cell Tissue Res 221(2), 351–359. https://doi.org/10.1007/BF00216739
Lewis KA, Tzilivakis J, Warner DJ, Green A, 2016. An international database for pesticide risk assessments and management. Hum Ecol Risk Assess 22(4), 1050-1064. https://doi.org/10.1080/10807039.2015.1133242
Liao XL, Luo SD, Wu X, Wu J, 2011. Optimization of conditions for assaying activity of acetylcholinesterase in Bombus hypocrita (Hymenoptera: Apidae) and its sensitivity to six common insecticides. Acta Entomol Sin 54(12), 1361-1367. https://www.cabidigitallibrary.org/doi/full/10.5555/20123059620
Moritz RFA, Härtel S, Neumann P, 2005. Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity. Écoscience 12(3), 289-301. https://doi.org/10.2980/i1195-6860-12-3-289.1
Neov B, Georgieva A, Shumkova R, Radoslavov G, Hristov P, 2019. Biotic and abiotic factors associated with colonies mortalities of managed honey bee (Apis mellifera). Diversity 11, 237. https://doi.org/10.3390/d11120237
Porto RG, De Almeida RF, Cruz-Neto O, Tabarelli M, Viana BF, Peres CA, Lopes AV, 2020. Pollination ecosystem services: A comprehensive review of economic values, research funding and policy actions. Food Sec 12, 1425-1442. https://doi.org/10.1007/s12571-020-01043-w
Potts S, Biesmeijer K, Bommarco R, Breeze T, Carvalheiro L, Franzén M, González-Varo JP, Holzschuh A, Kleijn D, Klein A-M, et al., 2015. Status and trends of European pollinators. Key findings of the STEP project. Pensoft Publishers, Sofia, 72 pp. https://digital.csic.es/bitstream/10261/111215/1/STEP%20brochure.pdf
Ratnakar V, 2015. Safety evaluation of certain insecticides to European honeybee, Apis mellifera Linnaeus. Doctoral Thesis. Professor Jayashankar Telangana State Agricultural University, Hyderabad, India. https://krishikosh.egranth.ac.in/handle/1/92581
Rortais A, Arnold G, Dorne JL, More SJ, Sperandio G, Streissl F, Szentes C, Verdonck F, 2017. Risk assessment of pesticides and other stressors in bees: principles, data gaps and perspectives from the European Food Safety Authority. Sci Total Environ 587-588, 524-537. https://doi.org/10.1016/j.scitotenv.2016.09.127
Ruvolo-Takasusuki MCC, Ronqui L, Barateiro-Stuchi ALP, Araujo MC, Fermino F, Santos PR, de Toledo VDA, 2015. Biomonitoring the environmental quality by bees. In: Herbicides, physiology of action, and safety; Price A, Kelton J, Sarunaite L (eds.). pp: 97-122. InTech, Croatia. https://doi.org/10.5772/61616
Serra RS, Cossolin JFS, de Resende MTCS, de Castro MA, Oliveira AH, Martínez LC, Serrão JE, 2021. Spiromesifen induces histopathological and cytotoxic changes in the midgut of the honeybee Apis mellifera (Hymenoptera: Apidae). Chemosphere 270, 129439. https://doi.org/10.1016/j.chemosphere.2020.129439
Underwood E, Darwin G, Gerritsen E, 2017. Pollinator initiatives in EU Member States: Success factors and gaps. Report for European Commission under contract for provision of technical support related to Target 2 of the EU Biodiversity Strategy to 2020 – maintaining and restoring ecosystems and their services ENV.B.2/SER/2016/0018. Institute for European Environmental Policy, Brussels. https://ieep.eu/wp-content/uploads/2022/12/ieep_2017_pollinator_initiatives_in_eu_member_states.pdf
USDA, 2017. Attractiveness of agricultural crops to pollinating bees for the collection of nectar and/or pollen. https://www.ars.usda.gov/ARSUserFiles/OPMP/Attractiveness%20of%20Agriculture%20Crops%20to%20Pollinating%20Bees%20Report-FINAL_Web%20Version_Jan%203_2018.pdf
Visscher PK, Seeley TD, 1982. Foraging strategy of honeybee colonies in a temperate deciduous forest. Ecology 63(6), 1790-1801. https://doi.org/10.2307/1940121
Westphal C, Bommarco R, Carré G, Lamborn E, Morison N, Petanidou T, Potts SG, Roberts SPM, Szentgyörgyi H, Tscheulin T, et al., 2008. Measuring bee diversity in different European habitats and biogeographical regions. Ecol Monogr 78(4), 653-671. https://doi.org/10.1890/07-1292.1
Williamson SM, Moffat C, Gomersall MAE, Saranzewa N, Connolly CN, Wright GA, 2013. Exposure to acetylcholinesterase inhibitors alters the physiology and motor function of honeybees. Front Physiol 4, 13. https://doi.org/10.3389/fphys.2013.00013
Zanini S, Dainese M, Kopf T, Leitinger G, Tappeiner U, 2024. Maintaining habitat diversity at small scales benefits wild bees and pollination services in mountain apple orchards. Ecol Solutions Evidence 5(2), e12320. https://doi.org/10.1002/2688-8319.12320
Derechos de autor 2025 Consejo Superior de Investigaciones Científicas (CSIC)
Esta obra está bajo licencia internacional Creative Commons Reconocimiento 4.0.
© CSIC. Los originales publicados en las ediciones impresa y electrónica de esta Revista son propiedad del Consejo Superior de Investigaciones Científicas, siendo necesario citar la procedencia en cualquier reproducción parcial o total.
Salvo indicación contraria, todos los contenidos de la edición electrónica se distribuyen bajo una licencia de uso y distribución “Creative Commons Reconocimiento 4.0 Internacional ” (CC BY 4.0). Consulte la versión informativa y el texto legal de la licencia. Esta circunstancia ha de hacerse constar expresamente de esta forma cuando sea necesario.
No se autoriza el depósito en repositorios, páginas web personales o similares de cualquier otra versión distinta a la publicada por el editor.
