Skip to main content

Advertisement

Log in

Pollinator efficiency in openly grown eggplants: can non-vibrating bees produce high-quality fruits?

  • Original Paper
  • Published:
Arthropod-Plant Interactions Aims and scope Submit manuscript

Abstract

In the face of the global decline in pollinator populations, studies that serve as a basis for the conservation and management of crop pollinators are crucial. The eggplant (Solanum melongena) is a widely cultivated autogamous crop, whose production is favoured by pollination by vibrating (buzz pollinating bees). To our knowledge, thus far, no studies have tested for the pollination efficiency of non-vibrating bees, nor have any been conducted in semi-arid regions, or evaluated the influence of pollination on the chemical characteristics of the fruits. Here, we evaluated the influence of pollination by vibrating and non-vibrating pollinators on eggplant fruit set and fruit traits in two plantations within the semi-arid region of NE Brazil. We conducted 120 h of focal observations and compared the fruit set and size (weight, length, and basal and apical diameters) under different pollination treatments (open pollination, spontaneous self-pollination, hand-cross pollination and single visits by different species of pollinating bees). Nine visiting bee species were recorded, which differed in visiting frequency and behaviour, as well as in pollination efficiency. Although being autogamous, plants visited by the vibrating bee Xylocopa sp. set more fruits than open, spontaneous self- and cross-pollination. However, the fruits produced by Xylocopa sp. were lighter and smaller than those obtained through open pollination, highlighting the importance of multiple pollinator visits or pollinator diversity. Non-vibrating pollinators contributed to fruit production quantity and quality. Fruits resulting from open, hand cross-pollination and both vibrating (Euglossa sp. 1) and non-vibrating bees (Paratrigona sp.) were larger than those resulting from spontaneous self-pollination. Pollination treatments had no influence on fruit chemical properties. Our results highlight the importance of pollination to eggplant production and the benefits of both vibrating and non-vibrating pollinators.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Data availability

Not applicable.

Code availability

Not applicable.

References

  • Abak K, Sari N, Paksoy M, Kaftanoglu O, Yeninar H (1995) Efficiency of bumble bees on the yield and quality of eggplant and tomato grown in unheated glasshouses. Acta Hort 412:268–274

    Article  Google Scholar 

  • Abak K, Ozdogan AO, Dasgan HY, Derin K, Kaftanoglu O (2000) Effectiveness of bumble bees as pollinators for eggplants grown in unheated greenhouses. Acta Hort 514:97–203

    Google Scholar 

  • Association of Official Agricultural Chemist (AOAC) (1992) Official methods of analysis of the Association of the Agricultural Chemist, 11 edn. AOAC, Washinghton.

  • Barbosa MM, Carneiro LT, Pereira MFCS, Rodriguez CZ, Chagas TRF, Moya W et al (2020) Future scenarios of land-use-cover effects on pollination supply and demand in São Paulo State, Brazil. Biota Neotrop 20:e20190906

    Article  Google Scholar 

  • Bashir MA, Alvi AM, Khan KA, Rehmani MIA, Ansari MJ, Atta S et al (2018) Role of pollination in yield and physicochemical properties of tomatoes (Lycopersicon esculentum). Saudi J Biol Sci 25:1291–1297

    Article  PubMed  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Soft 67:1–48

    Article  Google Scholar 

  • Bezerra EL, Machado IC (2003) Biologia floral e sistema de polinização de Solanum stramonifolium. Acta Bot Bras 17:247–257

    Article  Google Scholar 

  • Bispo dos Santos SA, Roselino AC, Hrncir M, Bego LR (2009) Pollination of tomatoes by the stingless bee Melipona quadrifasciata and the honey bee Apis mellifera (Hymenoptera, Apidae). Gen Molec Research 8:751–757

    Article  Google Scholar 

  • Borges C, Anjos R, Silva T, Lima J, Andrade C (2012) Métodos de estimativa da evapotranspiração de referência diária para a microrregião de Garanhuns, PE. Rev Bras Eng Agr Amb 16:380–390

    Article  Google Scholar 

  • Branco RBF, Blatt SF (2014) Sistema de cultivo na produção de hortaliças. Pesq Tecna 11(1):1–6

    Google Scholar 

  • Brittain C, Williams N, Kremen C, Klein AM (2013) Synergistic effects of non-Apis bees and honey bees for pollination services. Proc Royal Soc B 280:20122767

    Article  Google Scholar 

  • Brody AL (1996) Envasado de alimentos en atmosferas controladas, modificadas y vacio. Acribia, Zaragoza

    Google Scholar 

  • Buchmann SL (1983) Buzz pollination, in angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination. Van Nostrand Reinhold, New York, pp 73–113

    Google Scholar 

  • Buchmann SL (2004) Buzz pollination in angiosperms. In: Jones CE, Little R (eds) Aspects of Centridine biology (Centris spp.) importance for pollination, and use of Xylocopa spp. as greenhouse pollinators of tomatoes and other crops. In: Freitas BM, Pereira JO (eds) Solitary bees: conservation, rearing and management for pollination. Imprensa Universitária, Fortaleza, pp 203–211

  • Burkart A, Lunau K, Schlindwein C (2011) Comparative bioacoustical studies on flight and buzzing of neotropical bees. J Poll Ecol 6:118–124

    Google Scholar 

  • Camargo JMF, Pedro SEM (2013) Meliponini Lepeletier, 1836. In: Moure JS, Urban D and Melo GAR (eds) catalogue of bees (Hymenoptera, Apoidea) in the Neotropical Region (Online). http://www.moure.cria.org.br/catalogue. Accessed 28 Oct 2020.

  • Cardinal S, Buchmann SL, Russell AL (2018) The evolution of floral sonication, a pollen foraging behavior used by bees (Anthophila). Evolution 72:590–600

    Article  PubMed  PubMed Central  Google Scholar 

  • Carvalheiro LG, Veldtman R, Shenkute AG, Tesfay GB, Pirk CWW, Donaldson JS et al (2011) Natural and within-farmland biodiversity enhances crop productivity. Ecol Letters 14:251–259

    Article  Google Scholar 

  • Carvalho DA, Oliveira PE (2003) Biologia reprodutiva e polinização de Senna sylvestris (Vell.) H.S. Irwin & Barneby (Leguminosae, Caesalpinioideae). Rev Bras Bot 26:319–328

    Article  Google Scholar 

  • Cauich O, Quezada Euan JJG, Ramírez VM, Valdovinos-Nuñez GR, Moo-Valle H (2006) Pollination of habanero pepper (Capsicum chinense) and production in enclosures using the stingless bee Nannotrigona perilampoides. J Apic Res 45:125–130

    Article  Google Scholar 

  • Chitarra MIF, Chitarra AB (2005) Pós-colheita de frutas e hortaliças: fisiologia e manuseio, 2nd edn. UFLA, Lavras.

  • Cooley H, Vallejo-Marín M (2021) Buzz-pollinated crops: a global review and meta-analysis of the effects of supplemental bee pollination in tomato. J Econ Entoml 114:505–519

    Article  CAS  Google Scholar 

  • Cruz DO, Campos LAO (2009) Polinização por abelhas em cultivos protegidos. Rev Bras Agroc 15:5–10

    Google Scholar 

  • Dafni A, Kevan PG, Husband BC (2005) Practical pollination biology. Enviroquest Ltd, Cambridge

    Google Scholar 

  • De Luca PA, Vallejo-Marín M (2013) What’s the “buzz” about? The ecology and evolutionary significance of buzz-pollination. Curr Op Pl Biol 16:429–435

    Article  Google Scholar 

  • De Luca PA, Bussière LF, Souto-Vilaros D, Goulson D, Mason AC, Vallejo-Marín M (2013) Variability in bumblebee pollination buzzes affects the quantity of pollen released from flowers. Oecologia 172:805–816

    Article  PubMed  Google Scholar 

  • Dellinger AS, PenneysDS SYM, Fragner L, Weckwerth W, Schönenberger J (2014) A specialized bird pollination system with a bellows mechanism for pollen transfer and staminal food body rewards. Curr Biol 24:1615–1619

    Article  CAS  PubMed  Google Scholar 

  • Eilers EJ, Kremen C, Smith Greenleaf S, Garber AK, Klein AM (2011) Contribution of pollinator-mediated crops to nutrients in the human food supply. PLoS ONE 6:e21363

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • EMBRAPA (Empresa Brasileira de Pesquisa Agroecuária) (2020) Cultivo da Berinjela. (Online). Embrapa Hortaliças (2007). https://www.embrapa.br/hortalicas/busca-de-solucoes-tecnologicas/-/produto-servico/1171/berinjela-cica/. Accessed 02 Feb 2020.

  • FAO (Food and Agriculture Organization of the United Nations) (2020) http://www.fao.org/faostat/en/#home. Accessed 20 Feb 2020

  • Fijen TPM, Scheper JÁ, Boekelo B, Raemakers I, Kleijn D (2019) Effects of landscape complexity on pollinators are moderated by pollinators’ association with mass-flowering crops. Proc Royal Soc B 286:20190387

    Article  Google Scholar 

  • Filgueira FAR (2000) Novo manual de olericultura: agrotecnologia moderna na produção e comercialização de hortaliças. UFV, Viçosa

  • Fründ J, Dormann CF, Holzschuh A, Tscharntke T (2013) Bee diversity effects on pollination depend on functional complementarity and niche shifts. Ecology 94:2042–2054

    Article  PubMed  Google Scholar 

  • Gallai N, Salles JM, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econom 68:810–821

    Article  Google Scholar 

  • Gharaghani A, Soloklui AKG, Oraguzie N, Zare D (2017) Pollen source influences fruit quality, aril properties, and seed characteristics in pomegranate. Int J Fruit Sci 17:333–348

    Article  Google Scholar 

  • Garibaldi LA, Marcelo A, Aizen UM, Alexandra M, Klein C, Saul A et al (2011) Global growth and stability of agricultural yield decrease with pollinator dependence. PNAS 108:5909–5914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garibaldi LA, Steffan-Dewenter I, Winfree R, Aizen MA, Bommarco R, Cunningham SA et al (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611

    Article  CAS  PubMed  Google Scholar 

  • Garibaldi LA, Carvalheiro LG, Vaissière BE, Gemmill-Herren B, Hipolito J, Freitas BM et al (2016) Mutually beneficial pollinator diversity and crop yield outcomes in small and large farms. Science 351:388–391

    Article  CAS  PubMed  Google Scholar 

  • Garófalo CA, Martins CF, Aguiar CML, Lama MAD, Alves-dos-Santos I (2012) As abelhas solitárias e perspectivas para seu uso na polinização no Brasil. In: Imperatriz-Fonseca VL et al (eds) Polinizadores do Brasil. Editora da Universidade de São Paulo, São Paulo, pp 183–203

    Google Scholar 

  • Gava, AJ, Silva CAB, Frias JR 2008 Tecnologia de alimentos: princípios e aplicações. Nobel, São Paulo

  • Gemmill-Herren B, Ochieng AO (2008) Role of native bees and natural habitats in eggplant (Solanum melongena) pollination in Kenya. Agric Ecosys Envi 127:31–36

    Article  Google Scholar 

  • George RAT (1999) Vegetable seed production, 2nd edn. University, Cambridge

    Google Scholar 

  • Giannini TC, Tambosi LR, Acosta AL, Jaffé R, Saraiva AM, Imperatriz-Fonseca VL et al (2015) Safeguarding ecosystem services: a methodological framework to buffer the joint effect of habitat configuration and climate change. PLoS ONE 10:e0129225

    Article  PubMed  PubMed Central  Google Scholar 

  • Greenleaf SS, Kremen C (2006) Wild bees enhance honey bees’ pollination of hybrid sunflower. PNAS 103:13890–13895

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guimarães BMC (2018) Polinização por abelhas em cultivo convencional e agroflorestal. Dissertação (Mestrado em Ciências Biológicas), Universidade Federal de Uberlândia, Uberlândia.

  • Harter B, Leistikow C, Wilms W, Truylio B, Engels W (2002) Bees collecting pollen from flowers with poricidal anthers in a south Brazilian Araucaria forest: a community study. J Apic Res 40:9–16

    Article  Google Scholar 

  • Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70

    Article  PubMed  Google Scholar 

  • IBGE (Instituto Brasileiro de Geografia e Estatística) (2012) Censo Agropecuário 2006 – Brasil, Grandes Regiões e Unidades da Federação, Segunda Apuração. IBGE, Rio de Janeiro

  • IPA (Instituto de Pesquisas Agropecuárias) (2008) Recomendações de adubação para o Estado de Pernambuco, 2nd edn. IPA, Recife PE

  • IPBES (edn) (2016) The assessment report of the Intergovernmental Science‐Policy Platform on Biodiversity and Ecosystem Services on pollinators, pollination and food production. In: Potts SG, Imperatriz‐Fonseca VL, Ngo HT (eds) Secretariat of the intergovernmental science‐policy platform on biodiversity and ecosystem services. Bonn, Germany (2016)

  • Kader AA (2008) Flavor quality of fruits and vegetables. J Sci Food Agric 88:1863–1868

    Article  CAS  Google Scholar 

  • Kevan PG, Eisikowitch D (1990) The effect of insect pollination on canola (Brassica napus L. cv. a.A.C. Triton) seed germination. Euphytica 45:39–41

    Article  Google Scholar 

  • Klatt BK, Holzschuh A, Westphal C, Clough Y, Smit I, Pawelzik E et al (2014) Bee pollination improves crop quality, shelf life and commercial value. Proc R Soc B 281:24–40

    Article  Google Scholar 

  • Klein AM, Vaissière BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C et al (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313

    Article  PubMed  Google Scholar 

  • Kowalska G (2006) Eggplant (Solanum melongena L.) flowering and fruiting dynamics depending on pistil type as well as way of pollination and flower harmonization. Folia Hort 18:17–29

    Google Scholar 

  • Kowalska G (2008) Flowering biology of eggplant and procedures intensifying fruit set—review. Acta Scient Polon Horotum Cultus 7:63–76

    Google Scholar 

  • Lenth RV (2016) Least-squares means: the R package lsmeans. J Stat Soft 69:1–33

    Article  Google Scholar 

  • Lowenstein DM, Minor ES (2015) Effect of number of Bombus impatiens (Hymenoptera: Apidae) visits on eggplant yield. J Econ Entom 108:1456–1459

    Article  PubMed  Google Scholar 

  • Martins KT, Gonzales A, Lechowicz MJ (2014) Pollination services are mediate by bee functional diversity and landscape context. Agric Ecos Envir 200:12–20

    Article  Google Scholar 

  • McGregor SE (1976) Insect pollination of cultivated crop plants. USDA, Washington, DC

    Google Scholar 

  • Monteiro TR (2018) Polinização por abelhas e a qualidade dos frutos em cultivos de berinjela (Solanum melongena, Solanaceae). Trabalho de Conclusão de Curso (Graduação em Ciências Biológicas) - Universidade Federal de Uberlândia, Uberlândia. 19 f

  • Montemor KA, Souza DTM (2009) Biodiversidade de polinizadores e biologia floral em cultura de berinjela (Solanum melongena). Zootec Trop 27:97–103

    Google Scholar 

  • Nunes-Silva P, Hrncir M, Imperatriz-Fonseca VLA (2010) Polinização Por Vibração. Oecol Austr 14:140–151

    Article  Google Scholar 

  • Nunes-Silva P, Hrncir M, Silva CI, Roldão YS, Imperatriz-Fonseca VL (2013) Stingless bees, Melipona fasciculata, as efficient pollinators of eggplant (Solanum melongena) in greenhouses. Apidologie 44:537–546

    Article  Google Scholar 

  • Osidacz RC, Ambrosio-Ugri MCB (2013) Physicochemical quality of eggplant dehydrated with varied pretreatments. Acta Scien Technol 35:175–179

    CAS  Google Scholar 

  • Patricio GB, Grisolia BB, Desuó IC, Montagnana PC, Brocanelli FG, Gomig EG et al (2012) The importance of bees for eggplant cultivations (Hymenoptera: Apidae, Andrenidae, Halictidae). Sociobiology 59:1037–1052

    Google Scholar 

  • Potts GS, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353

    Article  PubMed  Google Scholar 

  • Putra RE, Kinasih I (2014) Efficiency of Local Indonesia Honey Bees (Apis cerana L.) and Stingless Bee (Trigona iridipennis) on Tomato (Lycopersicon esculentum Mill.) Pollination. Pak J Biol Sci 17:86–91

    Article  PubMed  Google Scholar 

  • R Core Team (2019) A language and environment for statistical computing [Online]. Vienna, Austria. https://www.R-project.org.

  • Reifschneider F, Madeira MC, Ribeiro CSC (2003) Ciça: rende o ano inteiro. [Online]. Embrapa Hortaliças. https://www.embrapa.br/hortalicas/busca-de-solucoes-tecnologicas/-/produto-servico/1171/berinjela-cica/. Accessed 15 Feb 2020.

  • Reifschneideret FJB, Madeira MCB, Siva C (1993) Ciça: novo híbrido de berinjela resistente à antracnose e a podridão de fomopsis. Hort Bras 11:57

    Google Scholar 

  • Rosi‐Denadai CA, Araujo PCS, Campos LAO, Cosme L Jr, Guedes RNC (2018) Buzz‐pollination in Neotropical bees: genus‐dependent frequencies and lack of optimal frequency for pollen release. Insect Sci 1–10.

  • Sabara A, Gillespie DR, Elle E, Winston ML (2004) Influence of brood, vent screening, and time of year on honey bee (Hymenoptera: Apidae) pollination and fruit quality of greenhouse tomatoes. J Econ Entomol 97:727–734

    Article  CAS  PubMed  Google Scholar 

  • Santos AOR, Bartelli BF, Nogueira-Ferreira FH (2014) Potential pollinators of tomato, Lycopersicon esculentum (Solanaceae), in open crops and the effect of a solitary bee in fruit set and quality. J Econ Entom 107:987–994

    Article  CAS  PubMed  Google Scholar 

  • Schleuning M, Fründ J, García D (2015) Predicting ecosystem functions from biodiversity and mutualistic networks: an extension of trait-based concepts to plant–animal interactions. Ecography 38:380–392

    Article  Google Scholar 

  • Serrano AR, Guerra-Sanz JM (2006) Quality fruit improvement in sweet pepper culture by bumblebee pollination. Sci Hort 110:160–166

    Article  Google Scholar 

  • Silva CL, Freitas BM (2018) Rearing carpenter bees (Xylocopa spp.) for crop pollination: a case study with passion fruit (Passiflora edulis). In: DW Roubik. (Org.) The pollination of cultivated plants—a compendium for practitioners, 2 edn. FAO, Rome, v. 2, pp 89–100

  • Silva-Neto CM, Ribeiro ACC, Gomes FL, Melo APC, Oliveira GM, Faquinello P et al (2019) The stingless bee mandaçaia (Melipona quadrifasciata Lepeletier) increases the quality of greenhouse tomatoes. J Apic Res 58:9–15

    Article  Google Scholar 

  • Silveira FA, Melo GA,Almeida EA (2002) Abelhas brasileiras. Sistemática e Identificação. Fundação Araucária, Belo Horizonte.

  • Sousa FC et al (2013) Propriedades físicas e físico-químicas de polpa de juazeiro. Rev Verde Agroecol Desenvol Sustent 8(2):68–71

    Google Scholar 

  • Thorp RW (2000) The collection of pollen by bees. Pl Sys Evol 222:211–223

    Article  Google Scholar 

  • Vallejo-Marín M (2018) Buzz pollination: studying bee vibrations on flowers. New Phyt 224:1068–1074

    Article  Google Scholar 

  • Vallejo-Marín M (2019) Buzz pollination: studying bee vibrations on flowers. New Phyt 224:1068–1074

    Article  Google Scholar 

  • Vanommeslaeghe A, Meeus I, Cnops G, Vleugels T, Merchiers M, Duquenne B et al (2018) Influence of pollinator abundance and flower visitation on seed yield in red clover. Arthropod Pl Interac 12:339–349

    Article  Google Scholar 

  • Vieli L, Davis FW, Kendall BE, Altieri M (2016) Landscape effects on wild Bombus terrestris (Hymenoptera: Apidae) queens visiting highbush blueberry fields in south-central Chile. Apidologie 47:711–716

    Article  Google Scholar 

  • Zambon V, Agostini K (2017) Polimorfismo floral e suas implicações em sistemas sexuais: o caso de Solanum melongena (Solanaceae). Rodriguésia 68:1187–1199

    Article  Google Scholar 

  • Vaissière BE, Freitas BM, Gemmill-Herren B (2011) Protocol to detect and assess pollination deficits in crops: and assess pollination deficits in crops. FAO, Rome

    Google Scholar 

  • Vinícius-Silva R, Parma DF, Tostes RB, Arruda VM, Werneck MV (2017) Importance of bees in pollination of Solanum lycopersicum L. (Solanaceae) in open-field of the Southeast of Minas Gerais State. Brazil Hoehnea 44:349–360

    Article  Google Scholar 

  • Wille A (1963) Behavioral adaptations of bees for pollen collecting from Cassia flowers. Rev Biol Trop 11:205–210

    Google Scholar 

  • Wolowski M et al (2019) Relatório temático sobre polinização, polinizadores e produção de alimentos no Brasil, 1st edn. Cubo, São Carlos

    Book  Google Scholar 

Download references

Acknowledgements

We thank the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior for the scholarship granted to GPAC (grant code 001), the Conselho Nacional de Desenvolvimento Científico e Tecnológico for the research grant (428303/2018-8) and fellowship (309668/2018-2) given to CCC, the Programa de Pós-Graduação em Produção Agrícola of the Universidade Federal Rural de Pernambuco for the logistical and financial support, and the farmer for giving us permission to conduct the study on his property.

Funding

Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (grant code 001), Conselho Nacional de Desenvolvimento Científico (428303/2018–8 and 309668/2018–2).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Cibele Cardoso Castro.

Ethics declarations

Conflict of interest

The authors do not have conflicts of interest.

Ethics approval

Not applicable.

Informed consent

Not applicable.

Consent for publication

All authors agree to the publication of the manuscript.

Additional information

Communicated by Christina Mogren and Heikki Hokkanen.

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.

Supplementary file1 (DOCX 2550 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

de Araujo Campos, G.P., Barros, C.T., Carneiro, L.T. et al. Pollinator efficiency in openly grown eggplants: can non-vibrating bees produce high-quality fruits?. Arthropod-Plant Interactions 16, 159–170 (2022). https://doi.org/10.1007/s11829-022-09885-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11829-022-09885-1

Keywords

Navigation