Keywords
Dípteros; Himenópteros; comunidades de insectos; polinizadores; insectos visitantes de flores.
How to Cite
Abstract
Introduction: Wild plants rely mainly on insects for pollination, and many of these plants are essential to maintaining a diverse and abundant community of crop insect-pollinators. In Costa Rican highland ecosystems, the diversity and abundance of insect floral visitors have been poorly studied, despite their importance and proximity to crops in this area.
Objective: to determine the richness and composition of floral visitor insect species of native and ruderal herbaceous plants close to cultivated areas in San Gerardo de Dota, Costa Rica.
Methods: We systematically collected flower-visiting insects along transects in two different sites and identified them to the lowest taxonomic level. We estimated alpha diversity for each season and 11 plant groups created specifically for this study. We defined these plant groups based on flower morphology, life history traits, and their taxonomic relatedness. We also compared the insect community composition across seasons and plant groups.
Results: We collected a total of 1306 insects, mainly flies (Diptera), from 62 families on 46 plant species during 12 sampling visits. Insect diversity (alpha diversity) increased during the rainy season, possibly because resources (e.g., food and reproductive sites) for flies increase during this season. Insect species composition varied among plant groups. The most abundant insect communities overlapped extensively among plant groups, but other communities compose mainly by some tachinids, chloropids and wasps did not overlap between other plant groups.
Conclusion: Seasonal differences in flower-visiting insects could be attributed to a greater availability of resources during the rainy season. Differences in the composition of visitor insects across plant groups were likely influenced by temporal variation in blooming of the different plant groups, blooming intensity, and flower traits. To preserve the rich diversity of floral visitors and the pollination services they provide, a diverse array of ruderal plants must be maintained.
References
Aizen, M. A., Garibaldi, L. A., Cunningham, S. A., & Klein, A. M. (2008). Long-term global trends in crop yield and production reveal no current pollination shortage but increasing pollinator dependency. Current Biology, 18(20), 1572–1575. https://doi.org/10.1016/j.cub.2008.08.066
Alberdi, A., & Gilbert, M. T. P. (2019). A guide to the application of Hill numbers to DNA based diversity analyses. Molecular Ecology Resources, 19(4), 804–817. https://doi:10.1111/1755-0998.13014
Arroyo, M. T. K., Armesto, J. J., & Primack, R. B. (1984). Community studies in pollination ecology in the high temperate Andes of Central Chile II: effect of temperature on visitation rates and pollination possibilities. Plant Systems and Evolution, 149, 187–203. https://doi.org/10.1007/BF00983305
Baselga, A. (2023). Betapart: Partitioning Beta Diversity into Turnover and Nestedness Components. R package (Version 1.6) [Computer software]. CRAN. https://CRAN.R-project.org/package=betapart
Brenes, E. (2017). Analysis of the interactions of floral visitation by insects and their importance for the conservation of the flora of the páramo, in the Cerro de la Muerte Massif [Bachelor's Thesis, Universidad Estatal a Distancia, Costa Rica]. Researchgate. 10.13140/RG.2.2.14869.63207
Brown, B. V., Borkent, A., Cumming, J. M., Wood, D. M., Woodley, N. E., & Zumbado, M. A. (2009). Manual of Central America Diptera. (Vol. 1). NRC Research Press.
Brown, B. V., Borkent, A., Cumming, J. M., Wood, D. M., Woodley, N. E., & Zumbado, M. A. (2010). Manual of Central America Diptera. (Vol. 2). NRC Research Press.
Carvalheiro, L. G., Veldtman, R., Shenkute, A. G., Tesfay, G. B., Pirk, C. W. W. Donaldson, J. S., & Nicolson, S. W. (2011). Natural and within-farmland biodiversity enhances crop productivity. Ecology Letters, 14(3), 251–259. https://doi.org/10.1111/j.1461-0248.2010.01579.x
Chao, A. (1984). Nonparametric estimation of the number of classes in a population. Scandinavian Journal of Statistics, 11(4), 265–270. https://www.jstor.org/stable/4615964
Chao, A., Chiu, C. H., & Jost, L. (2014a). Unifying species diversity, phylogenetic diversity, functional diversity, and related similarity and differentiation measures through Hill numbers. Annual Review of Ecology, Evolution, and Systematics, 45, 297–324. https://doi.org/ 10.1146/annurev-ecolsys-120213-091540
Chao, A., Gotelli, N. J., Hsieh, T. C., Sander, E. L., Ma, K. H., Colwell, R. K., & Ellison, A. M. (2014b). Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecological Monographs, 84(1), 45–67. https://doi.org/10.1890/13-0133.1
Climate-data.org. (2021, December 18). Climate: San Gerardo de Dota, Costa Rica. Climate-data. https://es.climate-data.org/america-del-norte/costa-rica/san-jose/san-gerardo-de-dota-290308/
Cristóbal-Pérez, E. J., Barrantes, G., Cascante-Marín, A., Madrigal-Brenes, R., Hanson, P., & Fuchs, E. J. (2023). Blooming plant species diversity patterns in two adjacent Costa Rican highland ecosystems. PeerJ, 11, e14445. https://doi.org/10.7717/peerj.14445
Cristóbal-Pérez, E. J., Barrantes, G., Cascante-Marín, A., Hanson, P., Picado, B., Gamboa-Barrantes, N., Rojas-Malavasi, G., Zumbado, M. A., Madrigal-Brenes, R., Martén-Rodríguez, S., Quesada, M., & Fuchs, E J. (2024). Elevational and seasonal patterns of plant pollinator networks in two highland tropical ecosystems in Costa Rica. PLoS ONE, 19(1), e0295258. https://doi.org/10.1371/journal.pone.0295258
Da Paz, J. R. L., Gimenes, M., & Pigozzo, C. M. (2013). Three diurnal patterns of anthesis in Ipomoea carnea subsp. fistulosa (Convolvulaceae): Implications for temporal, behavioral and morphological characteristics of pollinators? Flora, 208(2), 138–146. https://doi.org/10.1016/j.flora.2013.02.007
Dellinger, A. S. (2020). Pollination syndromes in the 21st century: where do we stand and where may we go? New Phytologist, 228(4), 1193–1213. https://doi.org/10.1111/nph.16793
Dormann, C. F., Gruber, B., & Fruend, J. (2008). Introducing the bipartite Package: Analysing Ecological Networks. R news. 8(2), 8–11. https://journal.r-project.org/articles/RN-2008-010/
Dupont, Y. L., Hansen, D. M., & Olesen, J. M. (2003). Structure of a plant–flower-visitor network in the high-altitude sub-alpine desert of Tenerife Canary Islands. Ultrasound, 26(3), 301–310. https://doi.org/10.1034/j.1600-0587.2003.03443.x
Elberling, H. & Olesen, J. M. (1993). The structure of a high latitude plant–flower visitor system: the dominance of flies. Ultrasound, 22(3), 314–323. https://doi.org/10.1111/j.1600-0587.1999.tb00507.x
Fenster, C. B., Armbruster, W. S., Wilson, P., Dudash, M. R., & Thomson, J. D. (2004). Pollination Syndromes and Floral Specialization. Annual Review of Ecology, Evolution, and Systematics, 35(1), 375-403. https://doi.org/10.1146/annurev.ecolsys.34.011802.132347
Fontaine, C, Dajoz, I., Meriguet, J., & Loreau, M. (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biology, 4(1), e1. https://doi.org/10.1371/journal.pbio.0040001
Fontaine, C., Collin, C. L., & Dajoz, I. (2008). Generalist foraging of pollinators: Diet expansion at high density. Journal of Ecology, 96(5), 1002–1010. https://doi.org/10.1111/j.1365-2745.2008.01405.x
Garibaldi, L. A., Steffan-Dewenter, I., Winfree, R., Aizen, M. A., Bommarco, R., Cunningham, S. A., Kremen, C., Carvalheiro, L. G., Harder, L. D., Afik, O., Bartomeus, I., Benjamin, F., Boreux, V., Cariveau, D., Chacoff, N. P., Dudenhöffer, J. H., Freitas, B. M., Ghazoul, J., Greenleaf, S., Hipólito, J., ... Klein, A. M. (2013). Wild pollinators enhance fruit set of crops regardless of honeybee abundance. Science, 339(6127), 1608–1611. https://doi.org/10.1126/science.1230200
Hartshorn, G. S. (1991). Capítulo 7: Plantas. In D. H. Janzen (Ed.). Historia Natural de Costa Rica (pp. 118–353). Editorial de la Universidad de Costa Rica.
Herrera, C. M. (2019). Flower traits, habitat, and phylogeny as predictors of pollinator service: A plant community perspective. Ecological Monographs, 90(2), e01402. https://doi.org/10.1002/ecm.1402
Hoehn, P., Tscharntke, T., Tylianakis, J. M., & Steffan-Dewenter, I. (2008). Functional group diversity of bee pollinators increases crop yield. Proceedings of the Royal Society B, 275(1648), 2283–2291. https://doi.org/10.1098/rspb.2008.0405
Hsieh, T. C., Ma, K. H., & Chao, A. (2022). iNEXT: iNterpolation and EXTrapolation for species diversity (Version 3.0.0) [Computer software]. Retrieved from http://chao.stat.nthu.edu.tw/wordpress/software-download/
Inouye, D., Larson, B., Ssymank, A., & Kevan, P. (2015). Flies and flowers III: Ecology of foraging and pollination. Intelligent Transportation Systems Journal, 16(16), 115–133. https://doi.org/10.26786/1920-7603(2015)15
Ishikawa, Y., Kimura, M. T., & Toda, M. J. (2022). Biology and ecology of the Oriental flower-breeding Drosophila elegans and related species. Fly, 16(1), 207–220. https://doi.org/10.1080/19336934.2022.2066953
Janovský, Z. & Štenc, J. (2023). Pollinator community and generalisation of pollinator spectra changes with plant niche width and local dominance. Functional Ecology, 37(11), 1–10. 10.1111/1365-2435.14439
Jauker, F., & Wolters, V. (2008). Hoverflies are efficient pollinators of oilseed rape. Oecologia, 156(4), 819–823. doi:10.1007/s00442-008-1034-x
Junker, R. R., Blüthgen, N., Brehm, T., Binkenstein, J., Paulus, J., Schaefer, H. M., & Stang, M. (2013). Specialization on traits as basis for the niche-breadth of flower visitors and as structuring mechanism of ecological networks. Functional Ecology, 27(2), 329–341. https://doi.org/10.1111/1365-2435.12005
Kaiser-Bunbury, C. N., Muff, S., Memmott, J., Muller, C. B., & Caflisch, A. (2010). The robustness of pollination networks to the loss of species and interactions: a quantitative approach incorporating pollinator behaviour. Ecology Letters, 13(4), 442–452. https://doi.org/10.1111/j.1461-0248.2009.01437.x
Kearns, C. A. (1992). Anthophilous Fly Distribution Across an Elevation Gradient. The American Midland Naturalist, 127(1), 172–182. https://doi.org/10.2307/2426332
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 Royal the Society B, 274(1608), 303–313. https://doi.org/10.1098/rspb.2006.3721
Klein, A. M., Steffan-Dewenter, I., & Tscharntke, T. (2003). Fruit set of highland coffee increases with the diversity of pollinating bees. Proceedures Biological Sciences, 270(1518), 955–61. https://doi.org/10.1098/rspb.2002.2306
Kudo, G., Kohyama, T. I., Chen, K., Hsu, T., & Wang, C. (2023). Seasonal dynamics of floral composition and flower visitors in a subtropical alpine ecosystem in Taiwan. Ecological Research, 39(1), 27–41. https://doi.org/10.22541/au.168294629.96495497/v1
Lefebvre, V., Villemant, C., Fontaine, C., & Daugeron, C. (2018). Altitudinal, temporal and trophic partitioning of flower-visitors in Alpine communities. Scientific Reports, 8(4706), 1–11. https://doi.org/10.1038/s41598-018-23210-y
MacInnis, G., & Forrest, J. R. K. (2019). Pollination by wild bees yields larger strawberries than pollination by honeybees. Journal of Applied Ecology, 56(4), 824–832. https://doi.org/10.1111/1365-2664.13344
Maglianesi, M. A., Hanson, P., Brenes, E., Benadi, G., Schleuning, M., & Dalsgaard, B. (2020). High levels of phenological asynchrony between specialized pollinators and plants with short flowering phases. Ecology, 101(11), e03162. https://doi.org/10.1002/ecy.3162
Memmott, J., Craze, P. G., Waser, N. M., & Price, M. V. (2007). Global warming and the disruption of plant-pollinator interactions. Ecology Letters, 10(8), 710–717. https://doi.org/10.1111/j.1461-0248.2007.01061.x
Memmott, J., & Waser, N. M. (2002). Integration of alien plants into a native flower–pollinator visitation web. Proceedings of the Royal Society B, 269(1508), 23952399. http://doi.org/10.1098/rspb.2002.2174
Michener, C. D., McGinley, R. J., & Danforth, B. N. (1994). The Bee Genera of North and Central America (Hymenoptera: Apoidea). Smithsonian Institution, Washington, D.C.
Minachilis, K., Kougioumoutzis, K., & Petanidou, T. (2021). Climate change effects on multi-taxa pollinator diversity and distribution along the elevation gradient of Mount Olympus, Greece. Ecological Indicators, 132, 108335. https://doi.org/10.1016/j.ecolind.2021.108335
Montero B. K., Gamboa-Barrantes, N., Rojas-Malavasi, G., Cristóbal-Perez, E. J., Barrantes, G., Cascante-Marín, A., Hanson, P., Zumbado, M. A., Madrigal-Brenes, R., Martén-Rodríguez, S., Quesada, M., Fuchs, E. J. (2025). Pollen metabarcoding reveals a broad diversity of plant sources available to farmland flower visitors near tropical montane forest. Frontiers in Plant Science, 15, 1–13. https://doi.org/10.3389/fpls.2024.1472066
Oksanen, J., Blanchett, F. G., Friendly, M., Kindt, R., Legendre, P., McGlinn, Minchin, D. P. R., O'Hara, M. R. B., Simpson, G. L., Solymos, P., Stevens, M. H. H., Szoecs, E., & Wagner, H. (2020). Vegan: community ecology package. R package (Version 2.6-6.1) [Computer software]. CRAN. https://CRAN.R-project.org/package=vegan
Olesen, J. M., Bascompte, J., Elberling, H. & Jordano, P. (2008) Temporal dynamics in a pollination network. Ecology, 89(6), 1573–1582. https://doi.org/10.1890/07-0451.1
Ollerton, J., Killick, A., Lamborn, E., Watts, S., & Whiston, M. (2007). Multiple Meanings and Modes: On the Many Ways to Be a Generalist Flower. Taxon, 56(3), 717–728. https://doi.org/10.2307/25065856
Ollerton, J., Winfree, R., & Tarrant, S. (2011). How many flowering plants are pollinated by animals? Oikos, 120(3), 321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
Orford, K. A., Vaughan, I. P., & Memmott, J. (2015). The forgotten flies: the importance of non-syrphid Diptera as pollinators. Proceedings of Biological Science, 282(1805), 2014–2934. https://doi.org/10.1098/rspb.2014.2934
Pardo, A., Lopes, D. H., Fierro, N., & Borges, P. A. V. (2020). Limited Effect of Management on Apple Pollination: A Case Study from an Oceanic Island. Insects, 11(6), 351. https://doi.org/10.3390/insects11060351
Pérez-Méndez, N., Andersson, G. K. S., Requier, F., Hipólito, J., Aizen, M. A., Morales, C. L., García, N., Gennari, G. P., & Garibaldi, L. A. (2020). The economic cost of losing native pollinator species for orchard production. Journal of Applied Ecology, 57(3), 599–608. https://doi.org/10.1111/1365-2664.13561
Potts, S. G., Vulliamy, B., Dafni, A., Ne'eman, G., & Willmer, P. (2003), Linking Bees and Flowers: How Do Floral Communities Structure Pollinator Communities? Ecology 84(10), 2628–2642. https://doi.org/10.1890/02-0136
Primack, R. B. (1978). Variability in New Zealand montane and alpine pollinator assemblages. New Zealand Journal of Ecology, 1, 66–73. http://www.jstor.org/stable/24052382
R Core Team. (2024). R: A Language and Environment for Statistical Computing (Versión 4.3.3) [Computer software]. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/.
Reverté, S., Retana, J., Gómez, J. M. & Bosch, J. (2016). Pollinators show flower colour preferences but flowers with similar colours do not attract similar pollinators. Annals of Botany, 118(2), 249–57. https://doi.org/10.1093/aob/mcw103
Robinson, B. W., & Wilson, D. S. (1998). Optimal foraging, specialization, and a solution to Liem’s paradox. The American Naturalist, 151(3), 223–235. https://doi.org/10.1086/286113
Roswell, M., Dushoff, J., & Winfree, R. (2021). A conceptual guide to measuring species diversity. Oikos, 130, 321–338. https://doi.org/10.1111/oik.07202
Roubik, D. W. (1989). Ecology and natural history of tropical bees. Cambridge University Press, Cambridge, UK.
Santos, A. R. O., Lee, D. K., Ferreira, A. G., do Carmo, M. C., Rondelli, V. M., Barros, K. O., Hsiang, T., Rosa, C. A., & Lachance, M. A. (2020). The yeast community of Conotelus sp. (Coleoptera: Nitidulidae) in Brazilian passionfruit flowers (Passiflora edulis) and description of Metschnikowia amazonensis sp. nov., a large-spored clade yeast. Yeast, 37(3), 253–260. https://doi.org/10.1002/yea.3453
Schmitz, H. J., & Valente, V. L. D. S. (2019). The flower flies and the unknown diversity of Drosophilidae (Diptera): a biodiversity inventory in the Brazilian fauna. Papéis Avulsos de Zoologia, 59, e20195945. https://doi.org/10.11606/1807-0205/2019.59.45
Smith-Ramírez, C., Martinez, P., Nuñez, M., González, C., & Armesto, J. J. (2005). Diversity, flower visitation frequency and generalism of pollinators in temperate rain forests of Chiloe Island, Chile. Botanical Journal of the Linnean Society, 147(4), 399–416. https://doi.org/10.1111/j.1095-8339.2005.00388.x
Souza, C. S., Maruyama, P. K., Aoki, C., Sigrist, M. R., Raizer, J., Gross, C. L., & de Araujo, A. C. (2018). Temporal variation in plant–pollinator networks from seasonal tropical environments: Higher specialization when resources are scarce. Journal of Ecology, 106(6), 2409–2420. https://doi.org/10.1111/1365-2745.12978
Wickham, H. (2016). ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York. https://ggplot2.tidyverse.org
Wickham, H., Averick, M., Bryan, J., Chang, W., McGowan, L. D., François, R., Grolemund, G., Hayes, A., Henry, L., Hester, J., Kuhn, M., Pedersen, T. L., Miller, E., Bache, S. M., Müller, K., Ooms, J., Robinson, D., Seidel, D. P., Spinu, V.,…Yutani, H. (2019). “Welcome to the tidyverse.” Journal of Open Source Software, 4(43), 1686. https://doi.org/10.21105/joss.01686
Wickham, H., François, R., Henry, L., Müller, K., & Vaughan, D. (2023). dplyr: A Grammar of Data Manipulation (Version 1.1.3) [Computer software]. CRAN. https://CRAN.R-project.org/package=dplyr
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