Abstract
The honeybee (Apis mellifera) is one of the most important pollinator species because it can gather resources from a vast variety of plant species, including both natives and introduced, across its geographical distribution. Although A. mellifera interacts with a large diversity of plants and shares resources with other pollinators, there are some plant species with which it interacts more frequently than others. Here, we evaluated the plant traits (i.e., plant length, abundance of bloomed individuals, number of open flowers, and stamen length) that would affect the honeybee visit frequencies to the flowers in a coastal environment in the Gulf of Mexico. Moreover, we evaluated which native bee species (and their body size) overlap floral resource with A. mellifera. We registered 998 plant-bee interactions between 35 plant species and 47 bee species. We observed that plant species with low height and with high abundances of bloomed individuals are positively related to a high frequency of visits by A. mellifera. Moreover, we found that A. mellifera tends to share a higher number of plant species with other bee species with a similar or smaller body size than with bigger species, which makes them a competitor for the resource with honeybees. Our results highlight that the impacts of A. mellifera on plants and native bees could be anticipated based on its individual’s characteristics (i.e., plant height and abundance of bloomed individuals) and body size, respectively.
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References
Abou – Shaara HF (2014) The foraging behaviour of honey bees, Apis mellifera: a review. Vet Med 59(1):1–10
Aronne G, Giovanetti M, Guarracino MR, Micco V (2012) Foraging rules of flower selection applied by colonies of Apis mellifera: ranking and associations of floral sources. Funct Ecol 26(5):1186–1196. https://doi.org/10.1111/j.1365-2435.2012.02017.x
Bauer AA, Clayton MK, Brunet J (2017) Floral traits influencing plant attractiveness to three bee species: consequences for plant reproductive success. Am J Bot 104(5):772–781
Capellari A, Bonaldi G, Mei M, Paniccia D, Cerretti P, Marino L (2022) Functional traits of plants and pollinators explain resource overlap between honeybees and wild pollinators. Oecologia 198(4):1019–1029. https://doi.org/10.1007/s00442-022-05151-6
Casanelles-Abella J, Fontana S, Fournier B, Frey D, Moretti M (2021) Low resource availability drives feeding niche partitioning between wild bees and honeybees in a European city. Ecol Appl 33(1):e2727. https://doi.org/10.1002/eap.2727
Castillo-Campos G, Medina ME (2005) Arboles Y arbustos de la reserva natural de La Mancha, Veracruz, México. Manual para la identificación de especies. Veracruz, México Instituto de Ecología AC Xalapa
Duffield GE, Gibson RC, Gilhooly PM, Hesse AJ, Inkley CR, Gilbert FS, Barnard CJ (1993) Choice of flowers by foraging honey bees (Apis mellifera): possible morphological cues. Ecol Ent 18(3):191–197. https://doi.org/10.1111/j.1365-2311.1993.tb01089.x
Erickson E, Junker RR, Ali JG, McCartney N, Patch HM, Grozinger CM (2022) Complex floral traits shape pollinator attraction to ornamental plants. Ann Bot 130(4):561–577. https://doi.org/10.1093/aob/mcac082
Geslin B, Gauzens B, Thébault E, Dajoz I (2013) Plant Pollinator Networks along a gradient of urbanization. PLoS ONE 8(5):e63421. https://doi.org/10.1371/journal.pone.0063421
Giovanetti M, Aronne G (2011) Honey bee interest in flowers with anemophilous characteristics: first notes on handling time and routine on Fraxinus ornus and Castanea sativa B Insectol 64, 77–82
Goulson D (2003) Effects of introduced bees on native ecosystems. Annu Rev Ecol Evol Syst 34(1):1–26. https://doi.org/10.1146/annurev.ecolsys.34.011802.132355
Gu Z, Gu L, Eils R, Schlesner M, Brors B (2014) Circlize implements and enhances circular visualization in R. Bioinformatics 30(19):2811–2812. https://doi.org/10.1093/bioinformatics/btu393
Hernández-Yáñez H, Lara-Rodríguez N, Díaz-Castelazo C, Dáttilo W, Rico-Gray V (2013) Understanding the Complex structure of a Plant-Floral Visitor Network from different perspectives in Coastal Veracruz. Mexico Sociobiol 60(3):329–336. https://doi.org/10.13102/sociobiology.v60i3.329-336
Hubbell S (2001) The Unified Neutral Theory of Biodiversity and Bio- geography. Monographs in Population Biology. Princeton University Press, Princeton, New Jersey
Hung K-LJ, Kingston JM, Lee A, Holway DA, Kohn JR (2019) Non-native honey bees disproportionately dominate the most abundant floral resources in a biodiversity hotspot. Proc R Soc B 286:20182901. https://doi.org/10.1098/rspb.2018.2901
Kantsa A, Raguso RA, Dyer AG, Olesen JM, Tscheulin T, Petanidou T (2018) Disentangling the role of floral sensory stimuli in pollination networks. Nat Commun 9:1041. https://doi.org/10.1038/s41467-018-03448-w
Krishna A, Guimaraes PR, Jordano P, Bascompte J (2008) A neutral-niche theory of nestedness in mutualistic networks. Oikos 117:1609–1618. https://doi.org/10.1111/j.1600-0706.2008.16540.x
Leclercq G, Gengler N, Francis F (2018) How human reshaped diversity in honeybees (Apis mellifera L.): a review. Entomol Faun 71. https://doi.org/10.25518/2030-6318.4050
Leonhardt SD, Blüthgen N (2011) The same, but different: pollen foraging in honeybee and bumblebee colonies. Apidologie 43:449–464. https://doi.org/10.1007/s13592-011-0112-y
Luna P, Dáttilo W (2021) Disentangling plant-animal interactions into complex networks: a multi-view approach and perspec-tives. Plant-Animal Interactions: Source of Biodiversity, 1st edn. p 261–281
Luna P, García-Chávez JH, Izzo T, Sosa VJ, Del‐Claro K, Dáttilo W (2021b) Neutral and niche‐based factors simultaneously drive seed and invertebrate removal by red harvester ants. Ecol Entomol 46(4):816–826. https://doi.org/10.1111/een.13018
Lunau K, Maier EJ (1995) Innate colour preferences of flower visitors. J Comp Physiol A 177:1–19. https://doi.org/10.1007/BF00243394
MacInnis G, Normandin E, Ziter CD (2023) Decline in wild bee species richness associated with honey bee (Apis mellifera L.) abundance in an urban ecosystem. PeerJ 11:e14699. https://doi.org/10.7717/peerj.14699
Maia KP, Rasmussen C, Olesen JM, Guimaraes PR Jr (2019) Does the sociality of pollinators shape the organization of pollination networks? Oikos 128(5):741–752. https://doi.org/10.1111/oik.05387
Mallinger RE, Gaines-Day HR, Gratton C (2017) Do managed bees have negative effects on wild bees? A systematic review of the literature. PLoS ONE 12(12):e0189268. https://doi.org/10.1371/journal.pone.0189268
Manfredini F, Arbetman M, Toth AL (2019) A potential role for phenotypic plasticity in invasions and declines of social insects. Front Ecol Evol 7:375. https://doi.org/10.3389/fevo.2019.00375
Menezes Pedro SR, Camargo JMF (1991) Interactions on floral resources between the africanized honey bee Apis mellifera L and the native bee community (Hymenoptera: Apoidea) in a natural cerrado. Ecosyst Southeast Brazil Apidologie 22:397–415. https://doi.org/10.1051/apido:19910405
Moreno-Casasola P (2006) Entornos veracruzanos: La costa De La Mancha. Instituto de Ecología, AC Xalapa
Osterman J, Aizen MA, Biesmeijer JC, Bosch J, Howlett BG, Inouye DW, Jung C, Martins DJ, Medel R, Pauw A, Seymour CL, Paxton RJ (2021) Global trends in the number and diversity of managed pollinator species. Agric Ecosyst Environ 322:107653. https://doi.org/10.1016/j.agee.2021.107653
Paini DR (2004) Impact of the introduced honey bee (Apis mellifera) (Hymenoptera: Apidae) on native bees: a review. Austral Ecol 29(4):399–407. https://doi.org/10.1111/j.1442-9993.2004.01376.x
Parra-Tabla V, Angulo-Pérez D, Albor C, Campos-Navarrete MJ, Tun-Garrido J, Sosenski P, Alonso C, Ashman T-L, Arceo-Gómez G (2019) The role of alien species on plant-floral visitor network structure in invaded communities. PLoS ONE 14(11):e0218227. https://doi.org/10.1371/journal.pone.0218227
R Core Team (2016) R: A language and environment for statistical computing. (Version 4.0.2). Vienna, Austria: R Foundation for Statistical Computing. https://www.R-project.org/
Raiol RL, Gastauer M, Campbell AJ, Borges RC, Awade M, Giannini TC (2021) Specialist Bee species are larger and less phylogenetically distinct than generalists in Tropical Plant–Bee Interaction Networks. Front Ecol Evol 9:699649. https://doi.org/10.3389/fevo.2021.699649
Rasband WS, ImageJ US National Institutes of Health, Bethesda, Maryland, USA, https://imagej.nih.gov/ij/, 1997–2018
Rasmussen C, Dupont YL, Madsen HB, Bogusch P, Goulson D, Herbertsson L, Maia KP, Nielsen A, Olesen JM, Potts SG, Roberts SPM, Sydenham MAK, Kryger P (2021) Evaluating competition for forage plants between honey bees and wild bees in Denmark. PLoS ONE 16(4):e0250056. https://doi.org/10.1371/journal.pone.0250056
Ropars L, Affre L, Thébault E, Geslin B (2022) Seasonal dynamics of competition between honey bees and wild bees in a protected Mediterranean scrubland. Oikos 2022(4): e08915. 0.1111/oik.08915
Shimodaira H (2004) Approximately unbiased tests of regions using multistep-multiscale bootstrap resampling. Ann Stat 32(6):2616–2641. https://doi.org/10.1214/009053604000000823
Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22(12):1540–1542. https://doi.org/10.1093/bioinformatics/btl117
Weaver JR, Ascher JR, Mallinger RE (2022) Effects of short-term managed honeybee deployment in a native ecosystem on wild bee foraging and plant–pollinator networks. Insect Conserv Divers 15(5):634–644. https://doi.org/10.1111/icad.12594
Acknowledgements
This research was supported by the Consejo Nacional de Ciencia y Tecnología (CONACyT, Mexico) in 2022 under Grant No. FOP16-2021-01-319227 awarded to Wesley Dáttilo. Additionally, we want to thank to the Dr. Enrique César Crivelli for his technical support guidelines in the processing and identification of vegetal samples in the herbarium XAL at the Instituto de Ecología AC (INECOL).
Funding
This research was supported by the Consejo Nacional de Ciencia y Tecnología (CONACyT, Mexico) in 2022 under Grant No. FOP16-2021-01-319227 awarded to Wesley Dáttilo.
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CPC: conceived the study, sampling, data analysis, and wrote the manuscript. BR: sampling, data analysis, and reviewing and editing. FV: supervision and reviewing and editing. RA: bees’ taxonomic identification, and reviewing and editing. IH-D: supervision and reviewing and editing. WD: supervision, conceived the study, data analysis, and wrote the manuscript.
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Cruz, C.P., Ratoni, B., Villalobos, F. et al. Drivers of flower visit and resource sharing between the honeybee and native bees in Neotropical coastal sand dunes. Sci Nat 111, 2 (2024). https://doi.org/10.1007/s00114-024-01888-7
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DOI: https://doi.org/10.1007/s00114-024-01888-7