Hived native Cape honey bees provide a reliable and inexpensive pollination service for high-quality apple production in the Cape Floristic Region

Abstract

Pollination ecosystem service studies across multiple crops in many countries have shown that managed pollinators often complement wild pollinators. Such studies typically compare farms with or without access to wild pollinators, without controlling for the introduction of honey bee hives. Here, we compared three pollination strategies in commercial apple orchards in the Cape Floristic Region (CFR) of South Africa: (i) orchards relying exclusively on managed pollination through the introduction of hives of the endemic Cape honey bee (Apis mellifera capensis); (ii) orchards relying solely on pollination from all wild indigenous pollinators, including the Cape honey bee; and (iii) orchards using a combination of both sources. We found that pollination across all three pollination options was almost entirely from the Cape honey bee, but with significantly fewer flower visits in wild orchards. Wild pollinated orchards produced significantly fewer seeds per apple compared to orchards with hived honey bees, resulting in fewer apples of marketable size or shape. Hived bees resulted in the highest proportion of high-quality fruit. Summed across all farms, excluding insect pollination led to a ~95% reduction in the number of apples per tree, while in terms of apple marketability, failure to rent hives at 2 hives per hectare resulted in a 17.4-percentage-point reduction in high-quality fruit. Use of hived native honey bees in the CFR should therefore be considered an essential management input and an insurance measure for maintaining high-quality apple production. Our study emphasizes why local context should take precedence over broad international policy recommendations for optimal management of pollination services.

Keywords

Agroecosystem / Fruit set / Native honey bees / Apis mellifera capensis / Landscape context / Apple production / South Africa

Funding

This research was funded by the South African Department of Forestry, Fisheries and the Environment (DFFE). This publication does not necessarily represent the views or opinions of the DFFE or its employees. MJS was supported by the South African National Research Foundation.

Conflict of interest

The authors declare that they have no competing interests.

References

[1] Kremen C, Williams NM, Bugg RL, Fay JP, Thorp RW. The area requirements of an ecosystem service: crop pollination by native bee communities in California. Ecol Lett. 2004; 7:1109-1119. doi: 10.1111/j.1461-0248.2004.00662.x

[2] Chacoff NP, Aizen MA. Edge effects on flower-visiting insects in grapefruit plantations bordering premontane subtropical forest. J Appl Ecol. 2006; 43:18-27. doi: 10.1111/j.1365-2664.2005.01116.x

[3] Ricketts TH, Regetz J, Steffan-Dewenter I, et al. Landscape effects on crop pollination services: are there general patterns? Ecol Lett. 2008; 11:499-515. doi: 10.1111/j.1461-0248.2008.01157.x

[4] Klein AM, Brittain C, Hendrix SD, Thorp R, Williams N, Kremen C. Wild pollination services to California almond rely on semi-natural habitat. J Appl Ecol. 2012; 49:723-732. doi: 10.1111/j.1365-2664.2012.02144.x

[5] Rader R, Howlett BG, Cunningham SA, Westcott DA, Edwards W. Spatial and temporal variation in pollinator effectiveness: do unmanaged insects provide consistent pollination services to mass flowering crops? J Appl Ecol. 2012; 49:126-134. doi: 10.1111/j.1365-2664.2011.02066.x

[6] Garibaldi LA, Steffan-Dewenter I, Winfree R, et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science. 2013; 339:1608-1611. doi: 10.1126/science.1230200

[7] Rader R, Bartomeus I, Garibaldi LA, et al. Non-bee insects are important contributors to global crop pollination. Proc Natl Acad Sci USA. 2016; 113:146-151. doi: 10.1073/pnas.1517092112

[8] Winfree R, Williams NM, Dushoff J, Kremen C. Native bees provide insurance against ongoing honey bee losses. Ecol Lett. 2007; 10:1105-1113. doi: 10.1111/j.1461-0248.2007.01110.x

[9] Garibaldi LA, Steffan-Dewenter I, Kremen C, et al. Stability of pollination services decreases with isolation from natural areas despite honey bee visits. Ecol Lett. 2011; 14:1062-1072. doi: 10.1111/j.1461-0248.2011.01669.x

[10] Blitzer EJ, Gibbs J, Park MG, Danforth BN. Pollination services for apple are dependent on diverse wild bee communities. Agric Ecosyst Environ. 2016; 221:1-7. doi: 10.1016/j.agee.2016.01.004

[11] Klein AM, Vaissière BE, Cane JH, et al. Importance of pollinators in changing landscapes for world crops. Proc Biol Sci. 2007; 274:303-313. doi: 10.1098/rspb.2006.3721

[12] Aebi A, Vaissière BE, vanEngelsdorp D, Delaplane KS, Roubik DW, Neumann P. Back to the future: Apis versus non-Apis pollination: a response to Ollerton et al. Trends Ecol Evol. 2012; 27:142-143. doi: 10.1016/j.tree.2011.11.017

[13] Winfree R, Gross BJ, Kremen C.Valuing pollination services to agriculture. Ecol Econ. 2011; 71:80-88. doi: 10.1016/j.ecolecon.2011.08.001

[14] Cunningham SA, Fournier A, Neave MJ, Le Feuvre D. Improving spatial arrangement of honeybee colonies to avoid pollination shortfall and depressed fruit set. J Appl Ecol. 2016; 53:350-359. doi: 10.1111/1365-2664.12573

[15] Williams IH. The dependence of crop production within the European Union on pollination by honey bees. Agric Zool Rev. 1994; 6:229-257.

[16] Calderone NW.Insect pollinated crops, insect pollinators and US agriculture: Trend analysis of aggregate data for the period 1992-2009. PLoS One. 2012; 7:e37235. doi: 10.1371/journal.pone.0037235

[17] Mallinger RE, Gratton C. Species richness of wild bees, but not the use of managed honeybees, increases fruit set of a pollinator-dependent crop. J Appl Ecol. 2015; 52:323-330. doi: 10.1111/1365-2664.12377

[18] Rader R, Howlett BG, Cunningham SA, et al. Alternative pollinator taxa are equally efficient but not as effective as the honeybee in a mass flowering crop. J Appl Ecol. 2009; 46:1080-1087. doi: 10.1111/j.1365-2664.2009.01700.x

[19] Isaacs R, Williams N, Ellis J, Pitts-Singer TL, Bommarco R, Vaughan M. Integrated Crop Pollination: Combining strategies to ensure stable and sustainable yields of pollination-dependent crops. Basic Appl Ecol. 2017; 22:44-60. doi: 10.1016/j.baae.2017.07.003

[20] Vrdoljak S, Samways MJ, Simaika JP. Pollinator conservation at the local scale: flower density, diversity and community structure increase flower visiting insect activity to mixed floral stands. J Insect Conserv. 2016; 20:711-721. doi: 10.1007/s10841-016-9904-8

[21] Carvalheiro LG, Seymour CL, Veldtman R, Nicolson SW. Pollination services decline with distance from natural habitat even in biodiversity-rich areas. J Appl Ecol. 2010; 47:810-820. doi: 10.1111/j.1365-2664.2010.01829.x

[22] Allsopp MH, De Lange WJ, Veldtman R. Valuing insect pollination services with the cost of replacement. PLoS One. 2008; 3:e3128. doi: 10.1371/journal.pone.0003128

[23] Hortgro. Annual key deciduous fruit statistics. Compiled by the Hortgro for the South African Apple and Pear Producers’ Association; Paarl, South Africa; 2024. Available from: https://www.hortgro.co.za/wp-content/uploads/docs/dlm_uploads/2025/07/Pome-Fruit-2024-1.pdf [Last accessed on May 10, 2025].

[24] Gardee MN. Recovery of vegetation and bees after removal of pine forests after fire in the Limietberg region of the Cape Floristic Region biodiversity hotspot. Master’s thesis. University of Stellenbosch; 2015. Available from: https://scholar.sun.ac.za/browse/author?scope=22586279-cf6e-4d73-8cae-35951df25ab1&value=Gardee,%20Muhammed%20Nizaar&bbm.return=1 [Last accessed on June 22, 2025].

[25] Mucina L, Rutherford MC. The Vegetation of South Africa, Lesotho and Swaziland. Strelitzia 19. Pretoria: South African National Biodiversity Institute; 2006:478-479.

[26] Delaplane KS, Mayer DF. Crop Pollination by Bees. Wallingford, UK: CABI Publishing; 2001. doi: 10.1079/9780851994482.0000

[27] Davis K, Stover E, Wirth F. Economics of fruit thinning: A review focussing on apple and citrus. HortTechnology. 2004; 14:282-289. doi: 10.21273/HORTTECH.14.2.0282

[28] Zurbuchen A, Landert L, Klaiber J, Muller A, Hein S, Dorn S. Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol Conserv. 2010; 143(3):669-676. doi: 10.1016/j.biocon.2009.12.003

[29] Carvalheiro LG, Veldtman R, Shenkute A, et al. Natural and within-farmland biodiversity enhances crop productivity. Ecol Lett. 2011; 14:251-259. doi: 10.1111/j.1461-0248.2010.01579.x

[30] Hagler JR, Mueller S, Teuber LR, Machtley SA, Van Deynze A. Foraging range of honey bees, Apis mellifera, in alfalfa seed production fields. J Insect Sci. 2011; 11:144. doi: 10.1673/031.011.14401

[31] Eeraerts M, Meeus I, Van Den Berge S, Smagghe G. Landscapes with high intensive fruit cultivation reduce wild pollinator services to sweet cherry. Agric Ecosyst Environ. 2017; 239:342-348. doi: 10.1016/j.agee.2017.01.031

[32] Archive 2014 South African National Land-Cover. South African Biodiversity Institute, Biodiversity GIS. Available from: https://bgis.sanbi.org/dea_landcover [Last accessed on April 15, 2024].

[33] Johnson SD. Plant-animal relationships. In: Cowling RM,ed. The Ecology of Fynbos: Nutrients, Fire and Diversity. Cape Town, South Africa: Oxford University Press; 1992:411.

[34] Kuhlmann M. Patterns of diversity, endemism and distribution of bees (Insecta: Hymenoptera: Anthophila) in southern Africa. S Afr J Bot. 2009; 75:726-738. doi: 10.1016/j.sajb.2009.06.016

[35] Rebelo AG. Management implications. In: Rebelo AG,ed. A Preliminary Synthesis of Pollination Biology in the Cape Flora. Pretoria, South Africa: National Scientific Programmes Unit: CSIR, SANSP; 1987:265.

[36] Johannsmeier MF. Beekeeping in South Africa. Plant Protection Handbook No. 14. Pretoria, South Africa: Agricultural Research Council; 2001.

[37] Allsopp MH. Cape honeybee (Apis mellifera capensis Eschscholtz) and varroa mite (Varroa destructor Anderson and Trueman) threats to honeybees and beekeeping in Africa. Int J Trop Insect Sci. 2004; 24:87-94. doi: 10.1079/IJT20041

[38] Veldtman R. Are managed pollinators ultimately linked to the pollination ecosystem service paradigm? S Afr J Sci. 2018; 114(11/12). doi: 10.17159/sajs.2018/a0292

[39] De Marco P, Coelho FM. Services performed by the ecosystem: forest remnants influence agricultural cultures’ pollination and production. Biodivers Conserv. 2004; 13:1245-1255. doi: 10.1023/B:BIOC.0000019402.51193.e8

[40] Garratt MP, Breeze TD, Jenner N, Polce C, Biesmeijer JC, Potts SG. Avoiding a bad apple: Insect pollination enhances fruit quality and economic value. Agric Ecosyst Environ. 2014; 184:34-40. doi: 10.1016/j.agee.2013.10.032

[41] Bos MM, Veddeler D, Bogdanski AK, et al. Caveats to quantifying ecosystem services: fruit abortion blurs benefits from crop pollination. Ecol Appl. 2007; 17:1841-1849. doi: 10.1890/06-1763.1

[42] R Core Team. R: A Language and Environment for Statistical Computing. Vienna, Austria: R Foundation for Statistical Computing; 2005.

[43] Free JB. Insect Pollination of Crops. San Diego, CA, USA: Academic Press; 1993.

[44] Buccheri M, Di Vaio C. Relationship among seed number, quality, and calcium content in apple fruits. J Plant Nutr. 2005; 27:1735-1746. doi: 10.1081/PLN-200026409

[45] Matsumoto S, Soejima J, Maejima T. Influence of repeated pollination on seed number and fruit shape of ‘Fuji’ apples. Sci Hortic. 2012; 137:131-137. doi: 10.1016/j.scienta.2012.01.033

[46] Hoehn P, Tscharntke T, Tylianakis JM, Steffan-Dewenter I. Functional group diversity of bee pollinators increases crop yield. Proc R Soc Lond B Biol Sci. 2008; 275:2283-2291. doi: 10.1098/rspb.2008.0405

[47] Kleijn D, Winfree R, Bartomeus I, et al. Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat Commun. 2015; 6:1-8. doi: 10.1038/ncomms8414

[48] Isaacs R, Kirk AK. Pollination services provided to small and large highbush blueberry fields by wild and managed bees. J Appl Ecol. 2010; 47:841-849. doi: 10.1111/j.1365-2664.2010.01823.x

[49] Blaauw BR, Isaacs R. Flower plantings increase wild bee abundance and the pollination services provided to a pollination-dependent crop. J Appl Ecol. 2014; 51:890-898. doi: 10.1111/1365-2664.12257

[50] Ouma G. Fruit thinning with specific reference to citrus species: A review. Agric Biol J N Am. 2012; 3(4):175-191. doi: 10.5251/abjna.2012.3.4.175.191

[51] De Lange WJ, Veldtman R, Allsopp MH. Valuation of pollinator forage services provided by Eucalyptus cladocalyx. J Environ Manage. 2013; 125:12-18. doi: 10.1016/j.jenvman.2013.03.027

[52] Melin A, Rouget M, Midgley JJ, Donaldson JS. Pollination ecosystem services in South African agricultural systems. S Afr J Sci. 2014; 110(11/12):9. doi: 10.1590/sajs.2014/20140078

[53] Veldtman R, de Lange WJ. Valuing insect pollination services to safeguard crop pollination in South Africa. Insects. 2025; 16(12):1190. doi: 10.3390/insects16121190

[54] Syromiatnykov Y, Tursunova K, Ishniyazova S, Jaloliddin A. Physiology and immunity of honey bees (Apis mellifera) as a factor of disease resistance. AJBB. 2025; 2(9):114-123. doi: 10.51699/ajbb.v2i9.1499

[55] Ratto F, Steward P, Sait SM, et al. Proximity to natural habitat and flower plantings increases insect pollination services in South African apple orchards. J Appl Ecol. 2021; 58:2540-2551. doi: 10.1111/1365-2664.13984

[56] Garibaldi LA, Carvalheiro LG, Vaissière BE, et al. Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms. Science. 2016; 351(6271):388-391. doi: 10.1126/science.aac7287

[57] Bartomeus I, Potts SG, Steffan-Dewenter I, et al. Contribution of insect pollinators to crop yield and quality varies with agricultural intensification. PeerJ. 2014; 2:e328. doi: 10.7717/peerj.328

[58] Ghazoul J. Debating the Ecosystem Service Rationale for Conservation: Response to Kremen et al. Conserv Biol. 2008; 22:799-801. doi: 10.1111/j.1523-1739.2008.00941.x

[59] Kremen C, Daily GC, Klein AM, Scofield D. Inadequate assessment of the ecosystem service rationale for conservation: reply to Ghazoul. Conserv Biol. 2008; 22:795-798. doi: 10.1111/j.1523-1739.2008.00940.x

[60] De Palma A, Abrahamczyk S, Aizen MA, et al. Predicting bee community responses to land-use changes: Effects of geographic and taxonomic biases. Sci Rep. 2016; 6:31153. doi: 10.1038/srep31153