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Chemical composition of the ‘low quality’ pollen of sunflower (Helianthus annuus, Asteraceae)

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Abstract

The nutritional needs of bees are receiving renewed attention in the context of declining bee populations and changes in land use that threaten floral resources. We present a comprehensive analysis of the nutritional composition of sunflower (Helianthus annuus L.) pollen, comparing hand-collected, bee-collected and stored pollen. As found in previous studies, the protein content of sunflower pollen was relatively low compared to other important bee forage plants. In the cultivars tested, two essential amino acids, methionine and tryptophan, are likely to be below the minimum requirements for honeybees. Fatty acid composition showed lauric acid to be most abundant, followed by palmitic and α-linolenic acids. While sunflower offers abundant and accessible pollen, its quality may hinder bee development when it is an exclusive pollen source, and the cultivars of such mass-flowering crops may vary in value for pollinators.

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References

  • Alaux, C., Ducloz, F., Crauser, D., Le Conte, Y. (2010) Diet effects on honeybee immunocompetence. Biol. Lett. 6, 562–565

    Article  PubMed  Google Scholar 

  • Anderson, K.E., Sheehan, T.H., Eckholm, B.J., Mott, B.M., DeGrandi-Hoffman, G. (2011) An emerging paradigm of colony health: microbial balance of the honey bee and hive (Apis mellifera). Insectes Soc. 58, 431–444

    Article  Google Scholar 

  • AOAC (2000) Official methods of Analysis. Arlington, VA, USA

    Google Scholar 

  • Bidlingmeyer, B.A., Cohen, S.A., Tarvin, T.L. (1984) Rapid analysis of amino acids using pre-column derivatization. J. Chromatogr. 336, 93–104

    Article  PubMed  CAS  Google Scholar 

  • Carvalheiro, L.G., Veldtman, R., Shenkute, A.G., Tesfay, G.B., Pirk, C.W.W., Donaldson, J.S., Nicolson, S.W. (2011) Natural and within-farmland biodiversity enhances crop productivity. Ecol. Lett. 14, 251–259

    Article  PubMed  Google Scholar 

  • de Groot, A.P. (1953) Protein and amino acid requirements of the honey bee (Apis mellifica L.). Physiol. Comp. Oecol. 3, 1–83

    Google Scholar 

  • Farag, R.S., Youssef, A.M., Ewies, M.A., Hallabo, S.A.S. (1978) Long-chain fatty acids of six pollens collected by honeybees in Egypt. J. Apic. Res. 17, 100–104

    CAS  Google Scholar 

  • Feldlaufer, M.F., Knox, D.A., Lusby, W.R., Shimanuki, H. (1993) Antimicrobial activity of fatty acids against Bacillus larvae, the causative agent of American foulbrood disease. Apidologie 24, 95–99

    Article  CAS  Google Scholar 

  • Folch, J., Lees, M., Sloane Stanley, G.H. (1957) A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497–509

    PubMed  CAS  Google Scholar 

  • Free, J.B. (1964) The behaviour of honeybees on sunflowers (Helianthus annuus L.). J. Appl. Ecol. 1, 19–27

    Article  Google Scholar 

  • Genet, T., Labuschagne, M.T., Hugo, A. (2004) Capillary gas chromatography analysis of Ethiopian mustard to determine variability of fatty acid composition. J. Sci. Food Agric. 84, 1663–1670

    Article  CAS  Google Scholar 

  • Gilliam, M., McCaughey, W.F., Wintermute, B. (1980) Amino acids in pollens and nectars of citrus cultivars and in stored pollen and honey from honeybee colonies in citrus groves. J. Apic. Res. 19, 64–72

    CAS  Google Scholar 

  • González Paramás, A.M., Gómez Bárez, J.A., Cordón Marcos, C., García-Villanova, R.J., Sánchez-Sánchez, J. (2006) HPLC-fluorimetric method for analysis of amino acids in products of the hive (honey and bee-pollen). Food Chem. 95, 148–156

    Article  Google Scholar 

  • Herbert, E.W., Shimanuki, H. (1978) Chemical composition and nutritive value of bee-collected and bee-stored pollen. Apidologie 9, 33–40

    Article  Google Scholar 

  • Human, H., Nicolson, S.W. (2003) Digestion of maize and sunflower pollen by the spotted maize beetle Astylus atromaculatus (Melyridae): is there a role for osmotic shock? J. Insect Physiol. 49, 633–643

    Article  PubMed  CAS  Google Scholar 

  • Human, H., Nicolson, S.W. (2006) Nutritional content of fresh, bee-collected and stored pollen of Aloe greatheadii var. davyana (Asphodelaceae). Phytochemistry 67, 1486–1492

    Article  PubMed  CAS  Google Scholar 

  • Human, H., Nicolson, S.W., Strauss, K., Pirk, C.W.W., Dietemann, V. (2007) Influence of pollen quality on ovarian development in honeybees (Apis mellifera scutellata). J. Insect Physiol. 53, 649–655

    Article  PubMed  CAS  Google Scholar 

  • Kleinschmidt, G.J., Kondos, A.C. (1976) The influence of crude protein levels on colony production. Australian Beekeep. 80, 251–257

    Google Scholar 

  • Krause, G.L., Wilson, W.T. (1981) Honey bee pollination and visitation patterns on hybrid oilseed sunflowers in central Wyoming (Hymenoptera: Apidae). J. Kansas Entomol. Soc. 54, 75–82

    Google Scholar 

  • Leonhardt, S.D., Blűthgen, N. (2012) The same, but different: pollen foraging in honeybee and bumblebee colonies. Apidologie 43(4), 449–464

    Article  Google Scholar 

  • Loper, G.M., Cohen, A.C. (1987) Amino acid content of dandelion pollen, a honey bee (Hymenoptera: Apidae) nutritional evaluation. J. Econ. Entomol. 80, 14–17

    CAS  Google Scholar 

  • Loublier, Y., Ducruet, V., Pham-Delegue, M.-H., Douault, P., Vear, F., Degas, C., Masson, C. (1991) The pollen as an attraction parameter for pollinators to sunflower (Helianthus annuus L.). Acta Hort 288, 394–398

    Google Scholar 

  • Manning, R. (2001) Fatty acids in pollen: a review of their importance for honey bees. Bee World 82, 60–75

    Google Scholar 

  • Minckley, R.L., Wcislo, W.T., Yanega, D., Buchmann, S.L. (1994) Behavior and phenology of a specialist bee (Dieunomia) and sunflower (Helianthus) pollen availability. Ecology 75, 1406–1419

    Article  Google Scholar 

  • Müller, A., Kuhlmann, M. (2008) Pollen hosts of western palaearctic bees of the genus Colletes (Hymenoptera: Colletidae): the Asteraceae paradox. Biol. J. Linn. Soc. 95, 719–733

    Article  Google Scholar 

  • Nderitu, J., Nyamasyo, G., Kasina, M., Oronje, M.L. (2008) Diversity of sunflower pollinators and their effect on seed yield in Makueni District, Eastern Kenya. Span. J. Agric. Res. 6, 271–278

    Google Scholar 

  • Neff, J.L., Simpson, B.B. (1990) The roles of phenology and reward structure in the pollination biology of wild sunflower (Helianthus annuus L., Asteraceae). Isr. J. Bot. 39, 197–216

    Google Scholar 

  • Nicolson, S.W. (2011) Bee food: the chemistry and nutritional value of nectar, pollen and mixtures of the two. Afr. Zool. 46, 197–204

    Article  Google Scholar 

  • Peng, Y.-S., Nasr, M.E., Marston, J.M., Fang, Y. (1985) The digestion of dandelion pollen by adult worker honeybees. Physiol. Entomol. 10, 75–82

    Article  Google Scholar 

  • Pernal, S.F., Currie, R.W. (2000) Pollen quality of fresh and 1-year-old single pollen diets for worker honey bees (Apis mellifera L.). Apidologie 31, 387–409

    Article  Google Scholar 

  • Pham-Delègue, M.H., Etievant, P., Guichard, E., Marilleau, R., Douault, P.H., Chauffaille, J., Masson, C. (1990) Chemicals involved in honeybee–sunflower relationship. J. Chem. Ecol. 16, 3053–3065

    Article  Google Scholar 

  • Pierre, J., Mesquida, J., Marilleau, R., Pham-Delègue, M.H., Renard, M. (1999) Nectar secretion in winter oilseed rape, Brassica napus—quantitative and qualitative variability among 71 genotypes. Plant Breeding 118, 471–476

    Article  CAS  Google Scholar 

  • Rayner, C.J., Langridge, D.F. (1985) Amino acids in bee-collected pollens from Australian indigenous and exotic plants. Aust. J. Exp. Agric. 25, 722–726

    Article  CAS  Google Scholar 

  • Reinhard, A., Janke, M., von der Ohe, W., Kempf, M., Theuring, C., Hartmann, T., Schreier, P., Beuerle, T. (2009) Feeding deterrence and detrimental effects of pyrrolizidine alkaloids fed to honey bees (Apis mellifera). J. Chem. Ecol. 35, 1086–1095

    Article  PubMed  CAS  Google Scholar 

  • Roulston, T.H., Cane, J.H. (2000) Pollen nutritional content and digestibility for animals. Plant Syst. Evol. 222, 187–209

    Article  CAS  Google Scholar 

  • Roulston, T.H., Cane, J.H., Buchmann, S.L. (2000) What governs protein content of pollen: pollinator preferences, pollen–pistil interactions, or phylogeny? Ecol. Monogr. 70, 617–643

    Google Scholar 

  • Schmidt, J.O., Thoenes, S.C., Levin, M.D. (1987) Survival of honey bees, Apis mellifera (Hymenoptera: Apidae), fed various pollen sources. Ann. Entomol. Soc. Am. 80, 176–183

    Google Scholar 

  • Schmidt, L.S., Schmidt, J.O., Rao, H., Wang, W., Xu, L. (1995) Feeding preference and survival of young worker honey bees (Hymenoptera: Apidae) fed rape, sesame, and sunflower pollen. J. Econ. Entomol. 88, 1591–1595

    Google Scholar 

  • Schulz, S., Arsene, C., Tauber, M., McNeil, J.N. (2000) Composition of lipids from sunflower pollen (Helianthus annuus). Phytochemistry 54, 325–336

    Article  PubMed  CAS  Google Scholar 

  • Sedivy, C., Müller, A., Dorn, S. (2011) Closely related pollen generalist bees differ in their ability to develop on the same pollen diet: evidence for physiological adaptations to digest pollen. Funct. Ecol. 25, 718–725

    Article  Google Scholar 

  • Singh, S., Saini, K., Jain, K.L. (1999) Quantitative comparison of lipids in some pollens and their phagostimulatory effects in honey bees. J. Apic. Res. 38, 87–92

    CAS  Google Scholar 

  • Somerville, D.C. (2001) Nutritional value of bee collected pollens. Report for the Rural Industries Research and Development Corporation, Australia

    Google Scholar 

  • Somerville, D.C., Nicol, H.I. (2006) Crude protein and amino acid composition of honey bee-collected pollen pellets from south-east Australia and a note on laboratory disparity. Aust. J. Exp. Agric. 46, 141–149

    Article  CAS  Google Scholar 

  • Standifer, L.N. (1966) Fatty acids in dandelion pollen gathered by honey bees, Apis mellifera (Hymenoptera: Apidae). Ann. Entomol. Soc. Am. 59, 1005–1008

    CAS  Google Scholar 

  • Tasei, J.-N., Aupinel, P. (2008) Nutritive value of 15 single pollens and pollen mixes tested on larvae produced by bumblebee workers (Bombus terrestris, Hymenoptera: Apidae). Apidologie 39, 397–409

    Article  CAS  Google Scholar 

  • Tepedino, V.J., Parker, F.D. (1982) Interspecific differences in the relative importance of pollen and nectar to bee species foraging on sunflower. Env. Entomol. 11, 246–250

    Google Scholar 

  • Todd, F.E., Bretherick, O. (1942) The composition of pollens. J. Econ. Entomol. 35, 312–317

    CAS  Google Scholar 

  • Weiner, C.N., Hilpert, A., Werner, M., Linsenmair, K.E., Blüthgen, N. (2010) Pollen amino acids and flower specialisation in solitary bees. Apidologie 41, 476–487

    Article  Google Scholar 

  • Wille, H., Wille, M., Kilchenmann, V., Imdorf, A., Bűhlmann, G. (1985) Pollenerte und Massenwechsel von drei Apis mellifera-Vőlkern auf demselben Bienenstand in zwei aufeinanderfolgenden Jahren. Rev. Suisse Zool. 92, 897–914

    Google Scholar 

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Acknowledgements

Amino acid analyses were carried out at the Southern African Grain Laboratory in Pretoria and all other analyses at Nutrilab, University of Pretoria. We thank A.G. Shenkute and G.B. Tesfay for hel** with pollen collection, the National Research Foundation and the University of Pretoria for financial support, and the anonymous referees for useful comments.

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  1. Department of Zoology and Entomology, University of Pretoria, Pretoria, South Africa

    Susan Wendy Nicolson & Hannelie Human

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  1. Susan Wendy Nicolson
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Correspondence to Susan Wendy Nicolson.

Additional information

Composition chimique du pollen “de faible qualité” du tournesol ( Helianthus annuus Asteraceae)

Nutriments / protéine / lipides / acides aminés / acides gras

Chemische Zusammensetzung des „minderwertigen“Pollens der Sonnenblume ( Helianthus annuus , Asteraceae)

Nährstoffe / Proteine / Lipide / Aminosäuren / Fettsäuren

Manuscript editor: Yves Le Conte

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Nicolson, S.W., Human, H. Chemical composition of the ‘low quality’ pollen of sunflower (Helianthus annuus, Asteraceae). Apidologie 44, 144–152 (2013). https://doi.org/10.1007/s13592-012-0166-5

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  • DOI: https://doi.org/10.1007/s13592-012-0166-5

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