Abstract
Communities are characterized by the dominance of a few species, which are crucial for shaping communities. Bees compete for scarce resources, and offer an ideal system to study the effect of dominance on the diversity of bees. The effect of bee dominance is studied predominantly for the western honeybee, which often is illustrated negative in introduced sites. Solitary bees, stingless bees, native honeybees and bumblebees can also be dominant on flowers. We test the hypothesis that dominance, regardless of the identity of the species, negatively influence diversity of bees on flowers. We analyzed 95,160 visits of 58 species of bees on 59,211 flowers of 12 plant species for five years. Before the analyses, the visitors were grouped into honeybees, solitary bees, and stingless bees. Proportion of the total abundance accounted by the most abundant species was considered as the measure of dominance. Dominance was negatively associated with richness and visitation rate of bees, but identity of bee taxonomic group predicted the magnitude of the effects. Richness decreased with the dominance of honeybees and solitary bees, but not with the stingless bees. Visits of honeybees decreased when solitary bees dominated the visits. Visits of solitary bees decreased when honeybees or stingless bees dominated the flowers. We have shown that native bees of different taxonomic groups can exert a similar negative effect on bee diversity in flowers as invasive and managed species do. Honeybees and stingless bees, though native to some parts, deteriorate bee diversity if unnecessarily augmented to ecosystems for beekeeping.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Alroy J (2015) The shape of terrestrial abundance distributions. Sci Adv 1:e1500082
Angelella GM, McCullough CT, O’Rourke ME (2021) Honeybee hives decrease wild bee abundance, species richness, and fruit count on farms regardless of wildflower strips. Sci Rep 11:3202. https://doi.org/10.1038/s41598-021-81967-1
Ascher JS, Pickering J (2020) Discover life bee species guide and world checklist (Hymenoptera: Apoidea: Anthophila). http://www.discoverlife.org/mp/20q?guide=Apoidea_species
Avolio ML, Forrestel EJ, Chang CC, La Pierre KJ, Burghardt KT, Smith MD (2019) Demystifying dominant species. New Phytol 223:1106–1126. https://doi.org/10.1111/nph.15789
Badano EI, Vergara CH (2011) Potential negative effects of exotic honey bees on the diversity of native pollinators and yield of Highland coffee plantations. Agric Entomol 13:365–372. https://doi.org/10.1111/j.1461-9563.2011.00527.x
Balfour NJ, Garbuzov M, Ratnieks FLW (2013) Longer tongues and swifter handling: why do more bumble bees (Bombus spp.) than honeybees (Apis mellifera) forage on lavender (Lavandula Spp)? Ecol Entomol 38:323–329. https://doi.org/10.1111/een.12019
Balfour NJ, Gandy S, Ratnieks FL (2015) Exploitative competition alters bee foraging and flower choice. Behav Ecol Sociobiol 69:1731–1738. https://doi.org/10.1007/s00265-015-1985-y
Bartomeus I, Ascher JS, Gibbs J, Danforth BN, Wagner DL, Hedtke SM, Winfree R (2013) Historical changes in north eastern US bee pollinators related to shared ecological traits. Proc Natl Acad of Sci 110:4656–4660. https://doi.org/10.1073/pnas.1218503110
Bartoń K (2023) MuMIn: multi-model inference. R package version 1.47.5. https://CRAN.R-project.org/package=MuMIn
Bates D et al (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Biesmeijer JC, Roberts SP, Reemer M, Ohlemuller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers RJ, Thomas CD, Settele J (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354. https://doi.org/10.1126/science.1127863
Brown MJ, Paxton RJ (2009) The conservation of bees: a global perspective. Apidologie 40:410–416. https://doi.org/10.1051/apido/2009019
Campbell C, Russo L, Albert R, Buckling A, Shea K (2022) Whole community invasions and the integration of novel ecosystems. PLOS Comput Biol 18:e1010151.
Cunningham SA, Crane MJ, Evans MJ, Hingee KL, Lindenmayer DB (2022) Density of invasive western honeybee (Apis mellifera) colonies in fragmented woodlands indicates potential for large impacts on native species. Sci Rep 12:1–10. https://doi.org/10.1038/s41598-022-07635-0
Descamps C, Moquet L, Migon M, Jacquemart AL (2015) Diversity of the insect visitors on Calluna vulgaris (Ericaceae) in Southern France heathlands. J Insect Sci 15:130. https://doi.org/10.1093/jisesa/iev116
Dupont YL, Hansen DM, Valido A, Olesen JM (2004) Impact of introduced honeybees on native pollination interactions of the endemic Echium Wildpretii (Boraginaceae) on Tenerife, Canary Islands. Biol Conserv 118:301–311. https://doi.org/10.1016/j.biocon.2003.09.010
Eeraerts M, Vanderhaegen R, Smagghe G, Meeus I (2019) Pollination efficiency and foraging behaviour of honeybees and non-apis bees to sweet cherry. Agric for Entomol 22:75–82. https://doi.org/10.1111/afe.12363
Fox J et al (2016) Package ‘Car.’ An R package to applied regression. http://cran-r.project.org/web/packages/car/car.pdf
Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA, Kreman C, Carvalheiro LG, Harder LD, Afik O et al (2013) Wild pollinators enhance fruit set of crops regardless of honeybee abundance. Science 339:1608–1611
Garibaldi LA, Pérez-Méndez N, Cordeiro GD, Hughes A, Orr M, Alves‐dos‐Santos I, Freitas BM, Oliveira FF, LeBuhn G, Bartomeus I et al (2021) Negative impacts of dominance on bee communities: does the influence of invasive honeybees differ from native bees. Ecol 102:e03526. https://doi.org/10.1002/ecy.3526
Giannini TC, Garibaldi LA, Acosta AL, Silva JS, Maia KP, Saraiva AM, Guimaraes PR, Kleinert AM (2015) Native and non-native supergeneralist bee species have different effects on plant-bee networks. PLoS ONE 10:e0137198. https://doi.org/10.1371/journal.pone.0137198
Goras G, Tananaki C, Dimou M, Tscheulin T, Petanidou T, Thrasyvoulou A (2016) Impact of honeybee (Apis mellifera L.) density on wild bee foraging behaviour. J Apicul Sci 60:49–61. https://doi.org/10.1515/JAS-2016-0007
Goulson D, Nicholls E (2016) The canary in the coalmine; bee declines as an indicator of environmental health. Sci Prog 99:312326. https://doi.org/10.3184/003685016X14685000479908
Graystock P, Ng WH, Parks K, Tripodi AD, Muñiz PA, Fersch AA, Myers CR, McFrederick QS, McArt SH (2020) Dominant bee species and floral abundance drive parasite temporal dynamics in plant-pollinator communities. Nat Ecol Evol 4:1358–1367. https://doi.org/10.1038/s41559-020-1247-x
Grüter C, von Zuben LG, Segers FHID et al (2016) Warfare in stingless bees. Insect Soc 63:223–236
Hartig F, Hartig MF (2017) Package ‘DHARMa’:R package
Hejda M, Pyšek P, Jarošík V (2009) Impact of invasive plants on the species richness, diversity and composition of invaded communities. J Ecol 97:393–403. https://doi.org/10.1111/j.1365-2745.2009.01480.x
Hejda M, Sádlo J, Kutlvašr J, Petřík P, Vítková M, Vojík M, Pysek P, Pergl J (2021) Impact of invasive and native dominants on species richness and diversity of plant communities. Preslia 93:181–201. https://doi.org/10.23855/preslia.2021.181
Henry M, Rodet G (2018) Controlling the impact of the managed honeybee on wild bees in protected areas. Sci Rep 8:9308. https://doi.org/10.1038/s41598-018-27591-y
Herrera CM (2020) Gradual replacement of wild bees by honeybees in flowers of the Mediterranean Basin over the last 50 years. Proc R Soc B 287:20192657. https://doi.org/10.1098/rspb.2019.2657
Hudewenz A, Klein A-M (2013) Competition between honeybees and wild bees and the role of nesting resources in a nature reserve. J Insect Conserv 17:1275–1283. https://doi.org/10.1007/s10841-013-9609-1
Hudewenz A, Klein AM (2015) Red mason bees cannot compete with honeybees for floral resources in a cage experiment. Ecol Evol 21:5049–5056. https://doi.org/10.1002/ece3.1762
Hung KLJ, Kingston JM, Lee A, Holway DA, Kohn JR (2019) Non-native honeybees 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
Inouye DW (1978) Resource partitioning in bumble bees: experimental studies of foraging behaviour. Ecology 59:672–678
Isaacs R, Kirk AK (2010) Pollination services provided to small and large highbush blueberry fields by wild and managed bees. J Appl Ecol 47:841–849. https://doi.org/10.1111/j.1365-2664.2010.01823.x
Kennedy CM, Lonsdorf E, Neel MC, Williams NM, Ricketts TH, Winfree R, Bommarco R, Brittain C, Burley AL, Cariveau D, Carvalheiro LG (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599. https://doi.org/10.1111/ele.12082
Klaus F, Tscharntke T, Bischoff G, Grass I (2021) Floral resource diversification promotes solitary bee reproduction and may offset insecticide effects–evidence from a semi-field experiment. Ecol Lett 24:668–675. https://doi.org/10.1111/ele.13683
Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B: Biol Sci 274:303–313. https://doi.org/10.1098/rspb.2006.3721
Kovács-Hostyánszki A, Szigeti V, Miholcsa Z, Sándor D, Soltész Z, Török E, Fenesi A (2022) Threats and benefits of invasive alien plant species on pollinators. Basic Appl Ecol 64:89–102. https://doi.org/10.1016/j.baae.2022.07.003
Landaverde-González P, Quezada‐Euán JJG, Theodorou P, Murray TE, Husemann M, Ayala R, Moo-Valle H, Vandame R, Paxton RJ (2017) Sweat bees on hot chillies: provision of pollination services by native bees in traditional slash‐and‐burn agriculture in the Yucatán Peninsula of tropical Mexico. J Appl Ecol 54:1814–1824. https://doi.org/10.1111/1365-2664.12860
Leguizamón Y, Debandi G, Vázquez DP (2021) Managed honeybee hives and the diversity of wild bees in a dryland nature reserve. Apidologie 52:991–1001. https://doi.org/10.1007/s13592-021-00882-6
Lindström SA, Herbertsson L, Rundlöf M, Bommarco R, Smith HG (2016) Experimental evidence that honeybees depress wild insect densities in a flowering crop. Proc R Soc B: Biol Sci 283:20161641. https://doi.org/10.1098/rspb.2016.1641
Longo G, Seidler TG, Garibaldi LA, Tognetti PM, Chaneton EJ (2013) Functional group dominance and identity effects influence the magnitude of grassland invasion. J Ecol 101:1114–1124. https://doi.org/10.1111/1365-2745.12128
Lorenz S, Stark K (2015) Saving the honeybees in Berlin? A case study of the urban beekeeping boom. Envion Soc 1:116–126
MacInnis G, Normandin E, Ziter CD (2023) Decline in wild bee species richness associated with honey bee (Apismellifera L.) abundance in an urban ecosystem. PeerJ 3:11e14699. https://doi.org/10.7717/peerj.14699
Mallinger RE, Gratton C (2014) Species richness of wild bees, but not the use of managed honeybees, increases fruit set of a pollinator-dependent crop. J Appl Ecol 52:323–330. https://doi.org/10.1111/1365-2664.12377
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:e0189268. https://doi.org/10.1371/journal.pone.0189268
Michener CD (2007) The bees of the world, 2nd edn. John Hopkins University Press, Baltimore
Milner JR, Bloom EH, Crowder DW, Northfield TD (2020) Plant evolution can mediate negative effects from honeybees on wild pollinators. Ecol Evol 10:4407–4418. https://doi.org/10.1002/ece3.6207
Nabors AJ, Cen HJ, Hung KLJ, Kohn JR, Holway DA (2018) The effect of removing numerically dominant, non-native honeybees on seed set of a native plant. Oecologia 186:281–289. https://doi.org/10.1007/s00442-017-4009-y
Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. https://doi.org/10.1111/j.1600-0706.2010.18644.x
Paini DR, Roberts JD (2005) Commercial honeybees (Apis mellifera) reduce the fecundity of an Australian native bee (Hylaeus alcyoneus). Biol Conserv 123:103–112. https://doi.org/10.1016/j.biocon.2004.11.001
Potter DA, Mach BM (2022) Non-native Non-apis bees are more abundant on non-native Versus native flowering woody landscape plants. Insects 13:238. https://doi.org/10.3390/insects13030238
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007
Quezada-Euán JJG, May-Itzá WJ, de la Rúa P et al (2022) From neglect to stardom: how the rising popularity of stingless bees threatens diversity and meliponiculture in Mexico. Apidologie 53:70. https://doi.org/10.1007/s13592-022-00975-w
Rasmussen C (2013) Stingless bees (Hymenoptera: Apidae: Meliponini) of the Indian subcontinent: diversity, taxonomy and current status of knowledge. Zootaxa 3647:401–428. https://doi.org/10.11646/zootaxa.3647.3.1
Rasmussen C, Dupont YL, Madsen HB, Bogusch P, Goulson D, Herbertsson L, Maia KP, Nielsen A, Olesen JM, Potts SG, Roberts SP (2021) Evaluating competition for forage plants between honeybees and wild bees in Denmark. PLoS ONE 16:e0250056. https://doi.org/10.1371/journal.pone.0250056
Renner SS, Graf MS, Hentschel Z, Krause H, Fleischmann A (2021) High honeybee abundances reduce wild bee abundances on flowers in the city of Munich. Oecologia 195:825–831. https://doi.org/10.1007/s00442-021-04862-6
Requier F, Garnery L, Kohl PL, Njovu HK, Pirk CW, Crewe RM, Steffan-Dewenter I (2019) The conservation of native honeybees is crucial. Trends Ecol Evol 34:789–798. https://doi.org/10.1016/j.tree.2019.04.008
Rojas-Sandoval J, Ackerman JD, Marcano‐Vega H, Willig MR (2022) Alien species affect the abundance and richness of native species in tropical forests: the role of adaptive strategies. Ecosphere 13:e4291. https://doi.org/10.1002/ecs2.4291
Ropars L, Dajoz I, Fontaine C, Muratet A, Geslin B (2019) Wild pollinator activity negatively related to honeybee colony densities in urban context. PLoS ONE 14:e0222316. https://doi.org/10.1371/journal.pone.0222316
Ropars L, Affre L, Thébault É, Geslin B (2022) Seasonal dynamics of competition between honeybees and wild bees in a protected Mediterranean Scrubland. Oikos 2022:e08915. https://doi.org/10.1111/oik.08915
Roubik DW, Villanueva-Gutierrez R (2009) Invasive africanized honeybee impact on native solitary bees: a pollen resource and trap nest analysis. Biol J Linn Soc 98:152–160. https://doi.org/10.1111/j.1095-8312.2009.01275.x
Russo L, de Keyzer CW, Harmon-Threatt AN, LeCroy KA, MacIvor JS (2021) The managed-to-invasive species continuum in social and solitary bees and impacts on native bee conservation. Curr Opin Insect Sci 46:4349. https://doi.org/10.1016/j.cois.2021.01.001
Sinu PA, Shivanna KR (2007) Pollination ecology of cardamom (Elettaria cardamomum) in the western ghats, India. J Trop Ecol 23:493–496. https://doi.org/10.1017/S0266467407004191
Sinu N, Sinu PA (2022) Temporal consistency in foraging time and bouts of a carpenter bee in a specialized pollination system. Curr Sci 122:213–216. https://doi.org/10.18520/cs/v122/i2/213-216
Steffan-Dewenter I, Tscharntke T (2000) Resource overlap and possible competition between honeybees and wild bees in central Europe. Oecologia 122:288–296. https://doi.org/10.1007/s004420050034
Su R, Dai W, Yang Y, Wang X, Gao R, He M, Zhao C, Mu J (2022) Introduced honeybees increase host plant abundance but decrease native bumble bee species richness and abundance. Ecosphere 13:e4085. https://doi.org/10.1002/ecs2.4085
Thomson DM (2006) Detecting the effects of introduced species: a case study of competition between Apis and Bombus. Oikos 114:407418. https://doi.org/10.1111/j.2006.0030-1299.14604.x
Valido A, Rodríguez-Rodríguez MC, Jordano P (2019) Honeybees disrupt the structure and functionality of plant-pollinator networks. Sci Rep 9:4711. https://doi.org/10.1038/s41598-019-41271-5
Vanbergen AJ, Initiative TIP (2013) Threats to an ecosystem service: pressures on pollinators. Front Ecol Env 11:251–259. https://doi.org/10.1890/120126
Vilà M, Espinar JL, Hejda M, Hulme PE, Jarošík V, Maron JL, Pergl J, Schaffner U, Sun Y, Pyšek P (2011) Ecological impacts of invasive alien plants: a meta-analysis of their effects on species, communities and ecosystems. Ecol Lett 14:702–708. https://doi.org/10.1111/j.1461-0248.2011.01628.x
Wagner DL (2020) Insect declines in the anthropocene. Annu Rev of Entomo 65:457–480. https://doi.org/10.1146/annurev-ento-011019-025151
Weekers T, Marshall L, Leclercq N, Wood TJ, Cejas D, Drepper B, Hutchinson L, Mitches D, Molenberg J-M, Smagghe G, Vandamme P, Vereecken NJ (2022) Dominance of honeybees is negatively associated with wild bee diversity in commercial apple orchards regardless of management practices. Agric Ecosyst Environ 323:107697. https://doi.org/10.1016/j.agee.2021.107697
Whittaker RH (1965) Dominance and diversity in land plant communities. Science 147:250–260
Widhiono I, Sudiana E, Suryaningsih S (2022) Impact of introduction of managed honeybee colony on wild bee diversity and abundance in an agroecosystem in Indonesia. Biodivers J 23:1099–1104. https://doi.org/10.13057/biodiv/d230254
Wignall VR, Brolly M, Uthoff C, Norton KE, Chipperfield HM, Balfour NJ (2020) Exploitative competition and displacement mediated by eusocial bees: experimental evidence in a wild pollinator community. Behav Ecol Sociobiol 74:1–15. https://doi.org/10.1007/s00265-020-02924-y
Acknowledgements
The field work of this project was supported by a research grant (7170/AS) to PAS by the Science Engineering Research Board, New Delhi. SV thanks Kerala State Council for Science and Technology for a Ph.D. fellowship. We also thank the two anonymous referees for their constructive criticism in the original version of the manuscript.
Funding
The research was funded by the Science Engineering Research Board, New Delhi.
Author information
Authors and Affiliations
Contributions
RTP, MK and AG: assisted in field observations. JT: identified the bees. PAS: did analysis. SV and PAS: designed the study, collected data, and wrote the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by Jens Dauber.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Varma, S., Rajesh, T.P., Manoj, K. et al. Dominance and identity of the dominant bee drive bee diversity on flowers. Biodivers Conserv 33, 333–346 (2024). https://doi.org/10.1007/s10531-023-02751-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-023-02751-3