Journal of Chemical Ecology

, Volume 40, Issue 5, pp 476–483 | Cite as

Nectar Minerals as Regulators of Flower Visitation in Stingless Bees and Nectar Hoarding Wasps

  • Ohad Afik
  • Keith S. Delaplane
  • Sharoni Shafir
  • Humberto Moo-Valle
  • J. Javier G. Quezada-Euán


Various nectar components have a repellent effect on flower visitors, and their adaptive advantages for the plant are not well understood. Persea americana (avocado) is an example of a plant that secretes nectar with repellent components. It was demonstrated that the mineral constituents of this nectar, mainly potassium and phosphate, are concentrated enough to repel honey bees, Apis mellifera, a pollinator often used for commercial avocado pollination. Honey bees, however, are not the natural pollinator of P. americana, a plant native to Central America. In order to understand the role of nectar minerals in plant—pollinator relationships, it is important to focus on the plant’s interactions with its natural pollinators. Two species of stingless bees and one species of social wasp, all native to the Yucatan Peninsula, Mexico, part of the natural range of P. americana, were tested for their sensitivity to sugar solutions enriched with potassium and phosphate, and compared with the sensitivity of honey bees. In choice tests between control and mineral-enriched solutions, all three native species were indifferent for mineral concentrations lower than those naturally occurring in P. americana nectar. Repellence was expressed at concentrations near or exceeding natural concentrations. The threshold point at which native pollinators showed repellence to increasing levels of minerals was higher than that detected for honey bees. The results do not support the hypothesis that high mineral content is attractive for native Hymenopteran pollinators; nevertheless, nectar mineral composition may still have a role in regulating flower visitors through different levels of repellency.


Avocado Nannotrigona perilampoides Phosphorus Pollination Polybia Potassium Trigona (=Frieseomelitta) nigra Hymenoptera Apoidea Vespoidea 


  1. Adler LS (2000) The ecological significance of toxic nectar. Oikos 91:409–420CrossRefGoogle Scholar
  2. Adler LS, Irwin RE (2005) Ecological costs and benefits of defenses in nectar. Ecology 86:2968–2978CrossRefGoogle Scholar
  3. Afik O, Dag A, Kerem Z, Shafir S (2006a) Analyses of avocado (Persea americana) nectar properties and their perception by honey bees (Apis mellifera). J Chem Ecol 32:1949–1963PubMedCrossRefGoogle Scholar
  4. Afik O, Dag A, Shafir S (2006b) The effect of avocado (Persea americana) nectar composition on its attractiveness to honey bees (Apis mellifera). Apidologie 37:317–325CrossRefGoogle Scholar
  5. Afik O, Dag A, Shafir S (2007) The perception of avocado (Persea americana: Lauraceae) bloom by the honey bee (Apis mellifera: Hymenoptera). Entomol Gen 30:135–153CrossRefGoogle Scholar
  6. Afik O, Dag A, Shafir S (2008) Honeybee, Apis mellifera, round dance is influenced by trace components of floral nectar. Anim Behav 75:371–377CrossRefGoogle Scholar
  7. Bänziger H, Boongird S, Sukumalanand P, Bänziger S (2009) Bees (Hymenoptera: Apidae) that drink human tears. J Kansas Entomol Soc 82:135–150CrossRefGoogle Scholar
  8. Barclay RMR (2002) Do plants pollinated by flying fox bats (Megachiroptera) provide an extra calcium reward in their nectar? Biotropica 34:168–171CrossRefGoogle Scholar
  9. Bouchard S, Vonhof MJ, Fenton MB, Monette G (2000) Nutrient preferences of Brazilian hummingbirds. Wilson Bull 112:558–562CrossRefGoogle Scholar
  10. Can-Alonzo C, Quezada-Euan JJG, Xiu-Ancona P, Moo-Valle H, Valdovinos-Nunez GR, Medina-Peralta S (2005) Pollination of ‘criollo’ avocados (Persea americana) and the behaviour of associated bees in subtropical Mexico. J Apic Res 44:3–8Google Scholar
  11. Carroll SP, Moore L (1993) Hummingbirds take their vitamins. Anim Behav 46:817–820CrossRefGoogle Scholar
  12. Carter C, Shafir S, Yehonatan L, Palmer RG, Thornburg R (2006) A novel role for proline in plant floral nectars. Naturwissenschaften 93:72–79PubMedCrossRefGoogle Scholar
  13. Eardley CD, Mansell MW (1996) The natural occurrence of insect pollinators in an avocado orchard. SAAGA Yearbook 19:36–38Google Scholar
  14. Escuredo O, Seijo MC, Fernandez-Gonzalez M (2011) Descriptive analysis of Rubus honey from the north-west of Spain. Int J Food Sci Technol 46:2329–2336CrossRefGoogle Scholar
  15. Galen C (1983) The effect of nectar thieving ants on seedset in floral scent morphs of Polemonium viscosum. Oikos 41:245–249CrossRefGoogle Scholar
  16. Gazit S, Degani C (2002) Reproductive biology. In: Whiley AW, Schaffer B, Wolstenholme BN (eds) The avocado: Botany, production and uses. CAB International, Wallingford, pp 101–133CrossRefGoogle Scholar
  17. Hagler JR (1990) Honey bee (Apis mellifera L) response to simulated onion nectars containing variable sugar and potassium concentrations. Apidologie 21:115–121CrossRefGoogle Scholar
  18. Hagler JR, Buchmann SL (1993) Honey-bee (Hymenoptera, Apidae) foraging responses to phenolic-rich nectars. J Kansas Entomol Soc 66:223–230Google Scholar
  19. Hiebert SM, Calder WA (1983) Sodium, potassium, and chloride in floral nectars: energy-free contributions to refractive-index and salt balance. Ecology 64:399–402CrossRefGoogle Scholar
  20. Ish-Am G, Eisikowitch D (1998) Low attractiveness of avocado (Persea americana Mill.) flowers to honeybees (Apis mellifera L.) limits fruit set in Israel. J Hortic Sci Biotechnol 73:195–204Google Scholar
  21. Ish-Am G, Barrientos-Priego AF, Castaneda-Vildozola A, Gazit S (1999) Avocado (Persea americana Mill.) pollinators in its region of origin. Rev Chapingo Ser Hortic 5:137–143Google Scholar
  22. Johnson S, Hargreaves AL, Brown M (2006) Dark, bitter-tasting nectar functions as a filter of flower visitors in a bird-pollinated plant. Ecology 87:2709–2716PubMedCrossRefGoogle Scholar
  23. Junker R, Chung AYC, Bluthgen N (2007) Interaction between flowers, ants and pollinators: additional evidence for floral repellence against ants. Ecol Res 22:665–670CrossRefGoogle Scholar
  24. Kessler D, Baldwin IT (2006) Making sense of nectar scents: the effects of nectar secondary metabolites on floral visitors of Nicotiana attenuata. Plant J 49:840–854CrossRefGoogle Scholar
  25. Kessler D, Gase K, Baldwin IT (2008) Field experiments with transformed plants reveal the sense of floral scents. Science 321:1200–1202PubMedCrossRefGoogle Scholar
  26. Knight RJ (2002) History, distribution and uses. In: Whiley AW, Schaffer B, Wolstenholme BN (eds) The avocado: Botany, production and uses. CAB International, Wallingford, pp 1–14CrossRefGoogle Scholar
  27. Liu FL, Fu WJ, Yang DR, Peng YQ, Zhang XW, He JZ (2004) Reinforcement of bee-plant interaction by phenolics in food. J Apic Res 43:155–157Google Scholar
  28. Liu F, Chen J, Chai J, Zhang X, Bai X, He D, Roubik DW (2007) Adaptive functions of defensive plant phenolics and a non-linear bee response to nectar components. Funct Ecol 21:96–100CrossRefGoogle Scholar
  29. London-Shafir I, Shafir S, Eisikowitch D (2003) Amygdalin in almond nectar and pollen—facts and possible roles. Plant Syst Evol 238:87–95Google Scholar
  30. Lorenzon MCA, Matrangolo CAR (2005) Foraging on some nonfloral resources by stingless bees (Hymenoptera, Meliponini) in a Caatinga region. Braz J Biol 65:291–298PubMedCrossRefGoogle Scholar
  31. Nicolson SW, W.-Worswick PV (1990) Sodium and potassium concentrations in floral nectars in relation to foraging by honey bees. S Afr J Zool 25:93–96Google Scholar
  32. Perez-Balam J, Quezada-Euan JJG, Alfaro-Bates R, Medina S, McKendrick L, Soro A, Paxton RJ (2012) The contribution of honey bees, flies and wasps to avocado (Persea americana) pollination in southern Mexico. J Poll Ecol 8:42–47Google Scholar
  33. Petanidou T (2007) Ecological and evolutionary aspects of floral nectars in Mediterranean habitats. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 343–376CrossRefGoogle Scholar
  34. Plesser Y (2007) Factors that affect the attraction of bumblebees (Bombus terrestris) to the cotton plant (Gossypium spp.). M.Sc. Dissertation, The Hebrew University of JerusalemGoogle Scholar
  35. Rhoades DF, Bergdahl JC (1981) Adaptive significance of toxic nectar. Am Nat 117:798–803CrossRefGoogle Scholar
  36. Roubik DW (1989) Ecological and natural history of tropical bees. Cambridge University Press, New YorkCrossRefGoogle Scholar
  37. Shafir S (1996) Color discrimination conditioning of a wasp, Polybia occidentalis (Hymenoptera: Vespidae). Biotropica 28:243–251CrossRefGoogle Scholar
  38. Silva EM, Dean BB (2000) Effect of nectar composition and nectar concentration on honey bee (Hymenoptera: Apidae) visitations to hybrid onion flowers. J Econ Entomol 93:1216–1221PubMedCrossRefGoogle Scholar
  39. Singaravelan N, Nee’man G, Inbar M, Izhaki I (2005) Feeding responses of free-flying honeybees to secondary compounds mimicking floral nectars. J Chem Ecol 31:2791–2804PubMedCrossRefGoogle Scholar
  40. Soto VC, Maldonado IB, Gil RA, Peralta IE, Silva MF, Galmarini CR (2013) Nectar and flower traits of different onion male sterile lines related to pollination efficiency and seed yield of F1 hybrids. J Econ Entomol 106:1386–1394PubMedCrossRefGoogle Scholar
  41. Souza B, Roubik D, Barth O, Heard T, Enriquez E, Carvalho C, Villas-Bôas J, Marchini L, Locatelli J, Persano-Oddo L, Almeida-Muradian L, Bogdanov S, Vit P (2006) Composition of stingless bee honey: setting quality standards. Interciencia 31:867–875Google Scholar
  42. Stephenson AG (1981) Toxic nectar deters nectar thieves of Catalpa speciosa. Am Midl Nat 105:381–383CrossRefGoogle Scholar
  43. Tan K, Wang ZW, Yang MX, Fuchs S, Luo LJ, Zhang ZY, Li H, Zhuang D, Yang S, Tautz J, Beekman M, Oldroyd BP (2012) Asian hive bees, Apis cerana, modulate dance communication in response to nectar toxicity and demand. Anim Behav 84:1589–1594CrossRefGoogle Scholar
  44. Vit P, Persano-Oddo L, Marano ML, Salas de Mejiasc E (1998) Venezuelan stingless bee honeys characterized by multivariate analysis of physicochemical properties. Apidologie 29:377–389CrossRefGoogle Scholar
  45. Vithanage V (1990) The role of the European honeybee (Apis mellifera L.) in avocado pollination. J Hortic Sci 65:81–86Google Scholar
  46. Waller GD, Carpenter EW, Ziehl OA (1972) Potassium in onion nectar and its probable effect on attractiveness of onion flowers to honey bees. J Am Soc Hortic Sci 97:535–539Google Scholar
  47. White JW (1992) Honey. In: Graham JM (ed) The hive and the honey bee. Dadant and Sons, Hamilton, pp 869–925Google Scholar
  48. Wright GA, Baker DD, Palmer MJ, Stabler D, Mustard JA, Power EF, Borland AM, Stevenson PC (2013) Caffeine in floral nectar enhances a pollinator’s memory of reward. Science 339:1202–1204PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • Ohad Afik
    • 1
  • Keith S. Delaplane
    • 1
  • Sharoni Shafir
    • 2
  • Humberto Moo-Valle
    • 3
  • J. Javier G. Quezada-Euán
    • 3
  1. 1.Department of EntomologyUniversity of GeorgiaAthensUSA
  2. 2.B. Triwaks Bee Research Center, Department of EntomologyThe Hebrew University of JerusalemRehovotIsrael
  3. 3.Departamento de Apicultura, Campus Ciencias Biológicas y AgropecuariasUniversidad Autonoma de YucatanMerida-XmatkuilMéxico

Personalised recommendations