Hostname: page-component-78c5997874-xbtfd Total loading time: 0 Render date: 2024-11-17T16:16:16.920Z Has data issue: false hasContentIssue false

Foraging choices balanced between resource abundance and handling concerns: how the honeybee, Apis mellifera, select the flowers of Robinia pseudoacacia

Published online by Cambridge University Press:  16 July 2018

M. Giovanetti*
Affiliation:
Center for Ecology, Evolution and Environmental Changes (cE3c), Faculdade de Ciências da Universidade de Lisboa, Lisbon 1749-016, Portugal
*
Author for correspondence Tel: 0039 349 2874872 Fax: +351 217500028 E-mail: manuela.giovanetti@gmail.com

Abstract

Nectar is a main resource harvested by foraging honeybees: their ability in selecting among flowers is the key to optimize resource collection. This ability is expected to be the result of co-evolutionary traits between the plant and the pollinator visiting it; notwithstanding, novel interactions may occur between native and invasive species. Analysing foraging efforts, flexibility and individual constrains has to be taken into account. The foraging pattern of the ubiquitous honeybee on Robinia pseudoacacia, a North-American species widely naturalized in European countries, grounds a perfect case study. The plant shows papilionate flowers especially reach in nectar, but their tripping mechanism is difficult for the small/light-weight honeybee. Yet Apis mellifera is known to pay frequent and constant visits to them: in fact, one of the most appreciated unifloral honey is produced out of R. pseudoacacia. The aim of this study was to understand when and how the bees overcome physical constraints to succeed in flower visits, and to what extent this flexibility extend from the individual to the species. Data were collected in Italy, through focal observations of foraging individuals, nectar content measurements and experiments with manipulated inflorescences. Results clearly indicate that nectar content changes accordingly to the state of flowers (visited or unvisited), which also show slight changes in appearance. Foraging individuals, able to detect these differences, perform active choices preferentially selecting already-visited flowers: lower in nectar content but easier to manipulate. Even if the choice is primarily driven by handling constraints, individual experience and strength of stimuli are prompting visits also to unvisited flowers, notwithstanding a higher risk of failure in resource collection. Behavioural plasticity matching a satisfactory compromise grounds the decision that maximizes the intake of resource balanced with the effort to gain it.

Type
Research Papers
Copyright
Copyright © Cambridge University Press 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aronne, G., Giovanetti, M. & De Micco, V. (2012) Morphofunctional traits and pollination mechanisms of Coronilla emerus L. flowers (Fabaceae). The Scientific World Journal 2012, 381575.Google Scholar
Aronne, G., Giovanetti, M., Sacchi, R. & De Micco, V. (2014) From flower to honey bouquet: possible markers for the botanical origin of Robinia honey. The Scientific World Journal 2014, 547275.Google Scholar
Barbi, S. (2008) Studi di biologia riproduttiva per la conservazione di alcune specie vegetali dell'ambiente mediterraneo e per la valorizzazione di produzioni eco-compatibili. Unpublished Dissertation, Università di Napoli Federico II, Napoli.Google Scholar
Barrett, R. P., Mebrahtu, T. & Hanover, J. W. (1990) Black locust: a multi-purpose tree species for temperate climates. Advances in new crops. Timber Press, Portland, 278283.Google Scholar
Benard, J., Stach, S. & Giurfa, M. (2006) Categorization of visual stimuli in the honeybee Apis mellifera. Animal Cognition 9, 257270.Google Scholar
Cierjacks, A., Kowarik, I., Joshi, J., Hempel, S., Ristow, M., Lippe, M. & Weber, E. (2013) Biological flora of the British Isles: Robinia pseudoacacia. Journal of Ecology 101(6), 16231640.Google Scholar
Córdoba, S.A. & Cocucci, A.A. (2011) Flower power: its association with bee power and floral functional morphology in papilionate legumes. Annals of Botany, 108, 919931.Google Scholar
Cox, G.W. (2004) Alien species and Evolution: The Evolutionary Ecology of Exotic Plants, Animals, Microbes, and Interacting Native Species. Washington, DC, Island Press.Google Scholar
DAISIE European Invasive Alien Species Gateway (2008) Available online at http://www.europe-aliens.org/speciesTheWorst.do (accessed 26 March 2018).Google Scholar
Dedej, S. & Delaplane, K.S (2005) Net energetic advantage drives honeybees (Apis mellifera L.) to nectar larceny in Vaccinium ashei Reade. Behavavioural Ecology and Sociobiology 57, 398403.Google Scholar
DeGomez, T. & Wagner, M. R. (2001) Culture and use of black locust. HortTechnology 11(2), 279288.Google Scholar
Dobson, H.E., Groth, I. & Bergstrom, G. (1996) Pollen advertisement: chemical contrasts between whole-flower and pollen odors. American Journal of Botany 83(7), 877885.Google Scholar
Duffield, G.E., Gibson, R.C., Gilhooly, P.M., Hesse, A.J., Inkley, C.R., Gilbert, F.S. & Barnard, C.J. (1993) Choice of flowers by foraging honey bees (Apis mellifera): possible morphological cues. Ecological Entomology 18(3), 191197.Google Scholar
Faegri, K. & van der Pijl, L. (1971) The Principles of Pollination Ecology. Oxford, UK, Pergamon Press, Second Revised Edition.Google Scholar
Farkas, Á. & Zajácz, E. (2007) Nectar production for the Hungarian honey industry. The European Journal of Plant Science and Biotechnology 1(2), 125151.Google Scholar
Fischer, A., Bednar-Friedl, B., Langers, F., Dobrovodská, M., Geamana, N., Skogen, K. & Dumortier, M. (2011) Universal criteria for species conservation priorities? Findings from a survey of public views across Europe. Biological Conservation 144, 9981007.Google Scholar
Fülöp, A. & Menzel, R. (2000) Risk-indifferent foraging behaviour in honeybees. Animal Behavavior 60(5), 657666.Google Scholar
Galloni, M., Podda, L., Vivarelli, D. & Cristofolini, G. (2007) Pollen presentation, pollen-ovule ratios, and other reproductive traits in Mediterranean Legumes (Fam. Fabaceae – Subfam. Faboideae). Plant Systematic and Evolution 266, 147164.Google Scholar
Gil, M. (2010) Reward expectations in honeybees. Communicative and Integrative Biology 3(2), 95100.Google Scholar
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. Bulletin of Insectology 64(1), 7782.Google Scholar
Giovanetti, M. & Aronne, G. (2013) Honey bee handling behaviour on the papilionate flower of Robinia pseudoacacia L. Arthropod-Plant Interaction 7(1), 119124.Google Scholar
Giurfa, M. & Núñez, J. A. (1992). Honeybees mark with scent and reject recently visited flowers. Oecologia 89(1), 113117.Google Scholar
Gonzalez, A., Rowe, C. L., Weeks, P.J., Whittle, D., Gilbert, F.S. & Barnard, C.J. (1995) Flower choice by honey bees (Apis mellifera L.): sex-phase of flowers and preferences among nectar and pollen foragers. Oecologia, 101, 258264.Google Scholar
Goulson, D. (1999) Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspectives in Plant Ecology, Evolution and Systematics 2(2), 185209.Google Scholar
Goulson, D., Chapman, J.W. & Hughes, W.O.H. (2001) Discrimination of unrewarding flowers by bees: direct detection of rewards and use of repellent scent marks. Journal of Insect Behaviour 14(5), 669678.Google Scholar
Grüter, C., Moore, H., Firmin, N., Helanterä, H. & Ratnieks, F.L. (2011) Flower constancy in honey bee workers (Apis mellifera) depends on ecologically realistic rewards. Journal of Experimental Biology 214(8), 13971402.Google Scholar
Han, F., Wallberg, A. & Webster, M. T. (2012) From where did the Western honeybee (Apis mellifera) originate?. Ecology and Evolution 2(8), 19491957.Google Scholar
Huntley, J.C. (1990) Robinia pseudoacacia L. black locust. Silvics of North America 2, 755761.Google Scholar
Jackson, M.M., Turner, M.G. & Pearson, S.M. (2014) Logging legacies affect insect pollinator communities in Southern Appalachian Forests. Southeastern Naturalist 13(2), 317336.Google Scholar
Lavin, M. & Delgado, A. (1990) Pollen brush of Papilionoideae (Leguminosae): morphological variation and systematic utility. American Journal of Botany 77, 12941312.Google Scholar
Manetas, Y. & Petropuolou, Y. (2000) Nectar amount, pollen visit duration and pollination success in the Mediterranean shrub Cistus creticus. Annals of Botany 86(4), 815820.Google Scholar
Pacini, E. & Nepi, M. (2007) Nectar Production and Presentation. pp. 167214 in Nicolson, S.W., Nepi, M. & Pacini, E. (Eds) Nectaries and Nectar. Dordrecht, Springer.Google Scholar
Rejmánek, M. & Richardson, D.M. (2013) Trees and shrubs as invasive alien species – 2013 update of the global database. Diversity and Distribution 19, 10931094.Google Scholar
Richardson, D.M. & Rejmánek, M. (2011) Trees and shrubs as invasive alien species – a global review. Diversity and Distribution 17, 788809.Google Scholar
Sanderson, C.E., Orozco, B.S., Hill, P.S.M. & Wells, H. (2006) Honeybee (Apis mellifera ligustica) response to differences in handling time, rewards and flower colours. Ethology 112, 937946.Google Scholar
Seeley, T.D., Camazine, S. & Sneyd, J. (1991) Collective decision-making in honey bees: how colonies choose among nectar sources. Behavioural Ecology and Sociobiology 28(4), 277290.Google Scholar
Somme, L., Moquet, L., Quinet, M., Vanderplanck, M., Michez, D., Lognay, G. & Jacquemart, A. L. (2016) Food in a row: urban trees offer valuable floral resources to pollinating insects. Urban Ecosystems 19(3), 11491161.Google Scholar
Totland, O. & Matthews, I. (1998) Determinants of pollinator activity and flower preference in the early spring blooming Crocus vernus. Acta Oecologica 19(2), 155165.Google Scholar
Vítková, M., Müllerová, J., Sádlo, J., Pergl, J. & Pyšek, P. (2017) Black locust (Robinia pseudoacacia) beloved and despised: a story of an invasive tree in Central Europe. Forest Ecology and Management 384, 287302.Google Scholar
Ward, H.M. & Groom, P. (1905) pp. 1920 in Groom, P. (Ed.) Trees: a Handbook of Forest Botany for the Woodlands and the Laboratory (Vol. 3). At the University Press, Cambridge.Google Scholar
Wells, H. & Wells, P.H. (1983) Honey bee foraging ecology: optimal diet, minimal uncertainty or individual constancy? Journal of Animal Ecology 52(3), 829836.Google Scholar
Whitfield, C.W., Behura, S.K., Berlocher, S.H., Clark, A.G., Johnston, J.S., Sheppard, W.S., Smith, D.R., Suarez, A.V., Weaver, D. & Tsutsui, N.D. (2006) Thrice out of Africa: ancient and recent expansions of the honey bee, Apis mellifera. Science 314(5799), 642645.Google Scholar