A systemic fungicide might reduce the male genitalia of a stingless bee species by one-third
DOI:
https://doi.org/10.37486/2675-1305.ec05043Keywords:
bees, geometric morphometrics, larval development, male reproductive system, toxicological risk assessmentAbstract
Bees are essential pollinating insects that significantly contribute to crop production. However, the use of pesticides in modern agriculture has resulted in bees being exposed to a plethora of harmful substances. Larvae of bees are particularly susceptible to exposure, as they can consume contaminated larval food during development. This study opportunely examined the effects of fungicides and insecticides on the size and shape of the genitalia of Scaptotrigona bipunctata (Lepeletier, 1836) males (Hymenoptera: Apidae: Meliponini) during larval development when experimental design was structured to obtain female bees (workers). Therefore, the geometric morphometric analyses were based on male bees that opportunistically emerged. Our findings showed a significant difference in the size of the genitalia of S. bipunctata males exposed to a systemic fungicide during larval development, while the genital shape remained similar. Although the exact impact of these morphological changes on the reproductive success of S. bipunctata males is uncertain, they suggest an adverse effect of pesticides on bees.
Downloads
References
Adams, D. C.; Collyer, M. L.; Kaliontzopoulou, A.; Sherratt, E. (2017) Geomorph: software for geometric morphometric analyses. https://cran.r-project.org/web/packages/geomorph/index.html
Baptistella, A. R.; Souza, C. C. M.; Santana, W. C.; Soares, A. E. E. (2012) Techniques for the in vitro production of queens in stingless bees (Apidae, Meliponini). Sociobiology, 59(1): 297-310. doi: 10.13102/sociobiology.v59i1.685
Barbosa, W. F.; Smagghe, G.; Guedes, R. N. C. (2015) Pesticides and reduced-risk insecticides, native bees and pantropical stingless bees: pitfalls and perspectives. Pest Management Science, 71: 1049-1196. doi: 10.1002/ps.4025
Carneiro, L. S.; Martínez, L. C.; Gonçalves, W. G.; Santana, L. M.; Serrão, J. E. (2020) The fungicide iprodione affects midgut cells of non-target honey bee Apis mellifera workers. Ecotoxicology and Environmental Safety, 189: 109991. doi: 10.1016/j.ecoenv.2019.109991
Chakrabarti, P.; Rana, S.; Sarkar, S.; Smith, B.; Basu, P. (2014) Pesticide-induced oxidative stress in laboratory and field populations of native honey bees along intensive agricultural landscapes in two Eastern Indian states. Apidologie, 46: 107-129. doi: 10.1007/s13592-014-0308-z
European Commission (2015) Agriculture and the environment: Agriculture and pesticides [online] https://ec.europa.eu/agriculture/envir/pesticides/index_en.htm. Access on: 22.iv.2023
Galaschi-Teixeira, J. S.; Falcon, T.; Ferreira-Caliman, M. J.; Witter, S.; Francoy, T. M. (2018) Morphological, chemical, and molecular analyses differentiate populations of the subterranean nesting stingless bee Mourella caerulea (Apidae: Meliponini). Apidologie, 49: 367-377. doi: 10.1007/s13592-018-0563-5
Ihaka, R; Gentleman, R (1996) R: a language for data analysis and graphics. Journal of Computational and Graphical Statistics, 5(3): 299-314. doi: 10.2307/1390807
Kerr, W. E.; Zucchi, R.; Nakadaira, J. T.; Butolo, J. E. (1962) Reproduction in the social bees (Hymenoptera: Apidae). Journal of the New York Entomological Society, 70: 265-276. https://biostor.org/reference/171303
Klatt, B. K.; Holzschuh, A.; Westphal, C.; Clough, Y.; Smit, I.; Pawelzik, E.; Tscharntke T. (2014) Bee pollination improves crop quality, shelf life and commercial value. Proceedings of the Royal Society B: Biological Sciences, 281(1775): 20132440. doi: 10.1098/rspb.2013.2440
Klein, A-M.; Vaissière, B. E.; Cane, J. H.; Steffan-Dewenter, I.; Cunningham, S. A.; Kremen, C.; Tscharntke, T. (2007) Importance of pollinators in changing landscapes for world crops. Proceedings of the Royal Society B: Biological Sciences, 274(1608): 303-313. doi: 10.1098/rspb.2006.3721
Lima, C. B. S.; Nunes, L. A.; Carvalho, C. A. L.; Ribeiro, M. F.; Souza, B. A. Silva, C. S. B. (2016) Morphometric differences and fluctuating asymmetry in Melipona subnitida Ducke 1910 (Hymenoptera: Apidae) in different types of housing. Brazilian Journal of Biology, 76(4): 845-850. doi: 10.1590/1519-6984.01015
Maia, U. M.; Santos Júnior, J. E.; Molina, M.; Galaschi-Teixeira, J. S.; Carvalho, A. T.; Miranda, L. S., Imperatriz-Fonseca, V. L., Oliveira, G.; Giannini, T. C. (2022) Evidence for morphological and genetic structuring of Plebeia flavocincta (Apidae: Meliponini) populations in Northeast Brazil. Frontiers in Ecology and Evolution, 10: 1057624. doi: 10.3389/fevo.2022.1057624
Malaspina, O.; Silva-Zacarin, E. C. M. (2008) Cell markers for ecotoxicological studies in target organs of bees. Journal of Morphological Sciences, 23: 303-309.
Menezes, C.; Vollet-Neto, A.; Imperatriz-Fonseca, V. L. (2013) An advance in the in vitro rearing of stingless bee queens. Apidologie, 44: 491-500. doi: 10.1007/s13592-013-0197-6
Papaefthimiou, C.; Theophilidis, G. (2001) The cardiotoxic action of the pyrethroid insecticide deltamethrin, the azole fungicide prochloraz, and their synergy on the semi-isolated heart of the bee Apis mellifera macedonica. Pesticide Biochemistry and Physiology, 69(2): 77-91. doi: 10.1006/pest.2000.2519
R Core Team (2018) R: A language and environment for statistical computing. The R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/
Rohlf, F. J. (2005) tpsDig, digitize landmarks and outlines, version 2.05. Department of Ecology and Evolution. State University of New York. Stony Brook
Sanchez-Bayo, F.; Goka, K. (2014) Pesticide residues and bees - A risk assessment. PLoS One, 9(4): e94482. doi: 10.1371/journal.pone.0094482
Santos, C. F.; Souza-Santos, P. D; Blochtein, B. (2015) In vitro rearing of stingless bee queens and their acceptance rates into colonies. Apidologie, 47: 539-547. doi: 10.1007/s13592-015-0398-2
Santos, C. F.; Acosta, A. L.; Dorneles, A. L.; Souza-Santos, P. D.; Blochtein, B. (2016) Queens become workers: pesticides alter caste differentiation in bees. Scientific Reports, 6: 31605. doi: 10.1038/srep31605
Santos, C. F.; Otesbelgue, A.; Blochtein, B. (2018) The dilemma of agricultural pollination in Brazil: Beekeeping growth and insecticide use. PLoS One, 13(7): e0200286. doi: 10.1371/journal.pone.0200286
Schlager, S. (2017) Morpho and Rvcg - shape analysis in R. In: Zheng, G.; Li, S.; Szekely, G. (Eds.). Statistical shape and deformation analysis, pp. 217-256. Academic Press inc. doi: 10.1016/B978-0-12-810493-4.00011-0
Sim, S.; Reid, S. (1999) Statistical inference by confidence intervals: Issues of interpretation and utilization. Physical Therapy, 79(2): 186-195. doi: 10.1093/ptj/79.2.186
Simon-Delso, N.; San Martin, G.; Bruneau, E.; Hautier, L.; Medrzycki, P. (2017) Toxicity assessment on honey bee larvae of a repeated exposition of a systemic fungicide, boscalid. Bulletin of Insectology, 70: 83-90.
Velthuis, H. H. W.; Koedam. D.; Imperatriz-Fonseca, V. L. (2005) The males of Melipona and other stingless bees, and their mothers. Apidologie, 36(2): 169-185. doi: 10.1051/apido:2005014
Downloads
Additional Files
Published
How to Cite
Issue
Section
License
Copyright (c) 2023 Author(s)
This work is licensed under a Creative Commons Attribution 4.0 International License.
© The author(s) - Published by Sociedade Entomológica do Brasil
Funding data
-
Conselho Nacional de Desenvolvimento Científico e Tecnológico
Grant numbers 309542/2020-0;350679/2022-3 -
Fundação de Amparo à Pesquisa do Estado do Rio Grande do Sul
Grant numbers 20/2551-0000203-9