Journal of Insect Conservation

, Volume 19, Issue 5, pp 837–848 | Cite as

Early spring floral foraging resources for pollinators in wet heathlands in Belgium

  • Laura Moquet
  • Carolin Mayer
  • Denis Michez
  • Bernard Wathelet
  • Anne-Laure Jacquemart
ORIGINAL PAPER

Abstract

In temperate regions, foraging resources for pollinating insects are particularly important in early spring, especially for social insects like bumblebees that are initiating colonies. Heathlands, protected open habitats under EU law, provide floral resources (pollen and nectar) for a range of pollinating insects. In early spring, in Belgian heathlands, only two floral resources are available: willows Salix spp. (Salicaceae) and bilberry Vaccinium myrtillus (Ericaceae). Our objective was to assess whether these two plant species provide quantitative and qualitative resources during early spring. We examined the springtime activity of flower visitors on both S. x multinervis and V. myrtillus flowers in relation to sugar concentration and composition in nectar as well as composition of polypeptides and amino acids in pollen. The chemical composition of pollen differed significantly between the two plant species. Salix x multinervis offered pollen with higher polypeptide and essential amino acid contents than V. myrtillus. However, nectar quantities of V. myrtillus flowers were relatively high compared to S. x multinervis. During the overlapping flowering period of the two plant species, flower visitors seemed to favor high quality and easily accessible pollen of S. x multinervis species and visited V. myrtillus mainly for nectar resources.

Keywords

Willow Bilberry Bumblebees Solitary bees Pollen Nectar 

Notes

Acknowledgments

The authors thank Maryse Vanderplanck, Romain Moerman and Nathalie Roger (Laboratory of Zoology, University of Mons) for assistance during chemical analyses, Isabelle Van de Vreken (Unit of Biological and Industrial Chemistry, Gembloux, University of Liège) for amino acid analyses, Rudy Wattiez (Proteomic and Microbiology, University of Mons) for polypeptide analyses, Marie Warnier (CARI, UCL) for nectar analyses. Thanks to Michael Keith-Lucas (University of Reading) for help during pollen identification and thanks to Sami Yunus (Institute of Condensed Matter and Nanosciences, UCL) for the construction of the electric vibrators for pollen collection. We would like to thank the “Département de la Nature et des Forêts” for the permission to study in nature reserves and for the derogation concerning the sampling of plant and insect individuals. All our thanks to the two anonymous reviewers who improved the first version of the manuscript. The study was conducted in accordance with current Belgian laws. Funding was provided by FSR grant (“Fonds spéciaux de recherche”, UCL) and FNRS (« Fonds de la Recherche Scientifique » , Web Impact project, FRFC 2.4613.12).

References

  1. Aerts R, Heil GW (1993) Heathlands: patterns and processes in a changing environment. Kluwer Academic Publishers, DordrechtCrossRefGoogle Scholar
  2. Alaux C, Ducloz F, Crauser D, Le Conte Y (2010) Diet effects on honeybee immunocompetence. Biol Lett 6:562–565. doi: 10.1098/rsbl.2009.0986 PubMedCentralCrossRefPubMedGoogle Scholar
  3. Baker HG, Baker I (1983) Floral nectar sugar constituents in relation to pollinator type. In: Jones CE, Little RJ (eds) Handbook of Experimental pollination biology. Van Nostrand Reinhold, New York, pp 117–141Google Scholar
  4. Baker HG, Baker I (1990) The predictive value of nectar chemistry to the recognition of pollinator types. Isr J Bot 39:157–166. doi: 10.1080/0021213X.1990.10677140 Google Scholar
  5. Bennett AB, Isaacs R (2014) Landscape composition influences pollinators and pollination services in perennial biofuel plantings. Agric Ecosyst Environ 193:1–8. doi: 10.1016/j.agee.2014.04.016 CrossRefGoogle Scholar
  6. Benton T (2006) Bumblebees: the natural history and identification of the species found in Britain. Collins, LondonGoogle Scholar
  7. Biesmeijer JC, Roberts SPM, Reemer M et al (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313:351–354. doi: 10.1126/science.1127863 CrossRefPubMedGoogle Scholar
  8. Buchmann SL (1983) Buzz pollination in angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold, New York, pp 73–113Google Scholar
  9. Buchmann SL, Nabhan GP (1997) The Forgotten Pollinators. Island Press, Washington (DC)Google Scholar
  10. Carvalheiro LG, Kunin WE, Keil P et al (2013) Species richness declines and biotic homogenisation have slowed down for NW-European pollinators and plants. Ecol Lett 16:870–878. doi: 10.1111/ele.12121 PubMedCentralCrossRefPubMedGoogle Scholar
  11. Carvell C (2002) Habitat use and conservation of bumblebees (Bombus spp.) under different grassland management regimes. Biol Conserv 103:33–49. doi: 10.1016/S0006-3207(01)00114-8 CrossRefGoogle Scholar
  12. Carvell C, Westrich P, Meek WR et al (2006) Assessing the value of annual and perennial forage mixtures for bumblebees by direct observation and pollen analysis. Apidologie 37:326–340. doi: 10.1051/apido:2006002 CrossRefGoogle Scholar
  13. Clicheroux E (1957) L’évolution des terrains incultes en Belgique. Bull Inst Rech Économiques Soc 23:497–524Google Scholar
  14. Cnaani J, Thomson JD, Papaj DR (2006) Flower choice and learning in foraging bumblebees: effects of variation in nectar volume and concentration. Ethology 112:278–285. doi: 10.1111/j.1439-0310.2006.01174.x CrossRefGoogle Scholar
  15. Cook SM, Awmack CS, Murray DA, Williams IH (2003) Are honey bees’ foraging preferences affected by pollen amino acid composition? Ecol Entomol 28:622–627. doi: 10.1046/j.1365-2311.2003.00548.x CrossRefGoogle Scholar
  16. Corbet SA, Williams IH, Osborne JL (1991) Bees and the pollination of crops and wild flowers in the European Community. Bee World 72:47–59. doi: 10.1080/0005772X.1991.11099079 CrossRefGoogle Scholar
  17. Coudun C, Gégout J-C (2007) Quantitative prediction of the distribution and abundance of Vaccinium myrtillus with climatic and edaphic factors. J Veg Sci 18:517–524. doi: 10.1111/j.1654-1103.2007.tb02566.x CrossRefGoogle Scholar
  18. Davila YC, Elle E, Vamosi JC et al (2012) Ecosystem services of pollinator diversity: a review of the relationship with pollen limitation of plant reproduction. Botany 90:535–543. doi: 10.1139/b2012-017 CrossRefGoogle Scholar
  19. De Groot AP (1953) Protein and amino acid requirements of the honeybee (Apis mellifica L.). Physiol Comp Oecol 3:1–90Google Scholar
  20. De Luca PA, Vallejo-Marín M (2013) What’s the “buzz” about? The ecology and evolutionary significance of buzz-pollination. Curr Opin Plant Biol 16:429–435. doi: 10.1016/j.pbi.2013.05.002 CrossRefPubMedGoogle Scholar
  21. Descamps C, Moquet L, Migon M, Jacquemart A-L (2015) Diversity of the insect visitors on Calluna vulgaris (Ericaceae) in Southern France heathlands. J Insect Sci. doi: 10.1093/jisesa/iev116
  22. Development Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  23. Dötterl S, Füssel U, Jürgens A, Aas G (2005) 1,4-dimethoxybenzene, a floral scent compound in willows that attracts an oligolectic bee. J Chem Ecol 31:2993–2998. doi: 10.1007/s10886-005-9152-y CrossRefPubMedGoogle Scholar
  24. Dötterl S, Glück U, Jürgens A et al (2014) Floral reward, advertisement and attractiveness to honey bees in dioecious Salix caprea. PLoS ONE 9:e93421. doi: 10.1371/journal.pone.0093421 PubMedCentralCrossRefPubMedGoogle Scholar
  25. Eckhardt M, Haider M, Dorn S, Müller A (2013) Pollen mixing in pollen generalist solitary bees: a possible strategy to complement or mitigate unfavourable pollen properties? J Anim Ecol 83:588–597. doi: 10.1111/1365-2656.12168 CrossRefGoogle Scholar
  26. Elmqvist T, Ågren J, Tunlid A (1988) Sexual dimorphism and between-year variation in flowering, fruit set and pollinator behaviour in a boreal willow. Oikos 53:58–66. doi: 10.2307/3565663 CrossRefGoogle Scholar
  27. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. doi: 10.2307/30033784 CrossRefGoogle Scholar
  28. Forup ML, Henson KS, Craze PG, Memmott J (2007) The restoration of ecological interactions: plant–pollinator networks on ancient and restored heathlands. J Appl Ecol 45:742–752. doi: 10.1111/j.1365-2664.2007.01390.x CrossRefGoogle Scholar
  29. Füssel U (2007) Floral scent in Salix L. and the role of olfactory and visual cues for pollinator attraction of Salix caprea L. Universitat Bayreuth, GermanyGoogle Scholar
  30. Génissel A, Aupinel P, Bressac C et al (2002) Influence of pollen origin on performance of Bombus terrestris micro-colonies. Entomol Exp Appl 104:329–336. doi: 10.1046/j.1570-7458.2002.01019.x CrossRefGoogle Scholar
  31. Gilbert FS (1981) Foraging ecology of hoverflies: morphology of the mouthparts in relation to feeding on nectar and pollen in some common urban species. Ecol Entomol 6:245–262. doi: 10.1111/j.1365-2311.1981.tb00612.x CrossRefGoogle Scholar
  32. Gimingham CH (1972) Ecology of Heathlands. Chapman & Hall, LondonGoogle Scholar
  33. Goulson D, Hanley ME, Darvill B et al (2005) Causes of rarity in bumblebees. Biol Conserv 122:1–8. doi: 10.1016/j.biocon.2004.06.017 CrossRefGoogle Scholar
  34. Goulson D, Lepais O, O’Connor S et al (2010) Effects of land use at a landscape scale on bumblebee nest density and survival. J Appl Ecol 47:1207–1215. doi: 10.1111/j.1365-2664.2010.01872.x CrossRefGoogle Scholar
  35. Grixti JC, Wong LT, Cameron SA, Favret C (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biol Conserv 142:75–84. doi: 10.1016/j.biocon.2008.09.027 CrossRefGoogle Scholar
  36. Hanley ME, Franco M, Pichon S et al (2008) Breeding system, pollinator choice and variation in pollen quality in British herbaceous plants. Funct Ecol 22:592–598. doi: 10.1111/j.1365-2435.2008.01415.x CrossRefGoogle Scholar
  37. Harder LD (1985) Morphology as a predictor of flower choice by bumble bees. Ecology 66:198–210. doi: 10.2307/1941320 CrossRefGoogle Scholar
  38. Harris LF, Johnson SD (2004) The consequences of habitat fragmentation for plant-pollinator mutualisms. Int J Trop Insect Sci 24:29–43. doi: 10.1079/IJT20049 Google Scholar
  39. Haslett JR (1989) Adult feeding by holometabolous insects: pollen and nectar as complementary nutrient sources for Rhingia campestris (Diptera: Syrphidae). Oecologia 81:361–363. doi: 10.1007/BF00377084 CrossRefGoogle Scholar
  40. Hendrickx F, Maelfait J-P, Van Wingerden W et al (2007) How landscape structure, land-use intensity and habitat diversity affect components of total arthropod diversity in agricultural landscapes. J Appl Ecol 44:340–351. doi: 10.1111/j.1365-2664.2006.01270.x CrossRefGoogle Scholar
  41. Inouye DW (1978) Resource partitioning in bumblebees: experimental studies of foraging behavior. Ecology 59:672–678. doi: 10.2307/1938769 CrossRefGoogle Scholar
  42. Jacquemart AL (1992) Préliminaires sur la production de nectar chez trois espèces de Vaccinium. Apidologie 23:453–464. doi: 10.1051/apido:19920507 CrossRefGoogle Scholar
  43. Jacquemart A-L (1993) Floral visitors of Vaccinium species in the high Ardenne, Belgium. Flora 188:263–273Google Scholar
  44. Jacquemart A-L (2003) Floral traits of Belgian Ericaceae species: are they good indicators to assess the breeding systems? Belg J Bot 136:154–164. doi: 10.2307/20794527 Google Scholar
  45. Javorek SK, Mackenzie KE, Vander Kloet SP (2002) Comparative pollination effectiveness among bees (Hymenoptera: Apoidea) on lowbush blueberry (Ericaceae: Vaccinium angustifolium). Ann Entomol Soc Am 95:345–351CrossRefGoogle Scholar
  46. Kaiser-Bunbury CN, Memmott J, Müller CB (2009) Community structure of pollination webs of Mauritian heathland habitats. Perspect Plant Ecol Evol Syst 11:241–254. doi: 10.1016/j.ppees.2009.04.001 CrossRefGoogle Scholar
  47. Katoh N, Goto N, Iizumi S (1985) Sugar composition of nectar in flowers of Salix species. Sci Rep Res Inst Tohoku Univ 39:45–52Google Scholar
  48. Kleijn D, Raemakers I (2008) A retrospective analysis of pollen host plant use by stable and declining bumble bee species. Ecology 89:1811–1823. doi: 10.1890/07-1275.1 CrossRefPubMedGoogle Scholar
  49. Kosior A, Celary W, Olejniczak P et al (2007) The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41:79–88. doi: 10.1017/S0030605307001597 CrossRefGoogle Scholar
  50. Lack AJ (1982) The ecology of flowers of chalk grassland and their insect pollinators. J Ecol 70:773–790. doi: 10.2307/2260104 CrossRefGoogle Scholar
  51. Lambinon J, Verloove F (2012) Nouvelle flore de Belgique, du Grand-Duché de Luxembourg, du Nord de la France et des régions voisines, Sixième edn. Jardin botanique national de Belgique, MeiseGoogle Scholar
  52. MacKenzie KE, Eickwort GC (1996) Diversity and abundance of bees (Hymenoptera: Apoidea) foraging on highbush blueberry (Vaccinium corymbosum L.) in Central New York. J Kans Entomol Soc 69:185–194Google Scholar
  53. Mayer C, Michez D, Chyzy A et al (2012) The abundance and pollen foraging behaviour of bumble bees in relation to population size of whortleberry (Vaccinium uliginosum). PLoS ONE 7:e50353. doi: 10.1371/journal.pone.0050353 PubMedCentralCrossRefPubMedGoogle Scholar
  54. Moroń D, Szentgyörgyi H, Wantuch M et al (2008) Diversity of wild bees in wet meadows: implications for conservation. Wetlands 28:975–983. doi: 10.1672/08-83.1 CrossRefGoogle Scholar
  55. Morse DH (1977) Resource partitioning in bumble bees: the role of behavioral factors. Science 197:678–680. doi: 10.1126/science.197.4304.678 CrossRefPubMedGoogle Scholar
  56. Nagamitsu T, Yoneda M, Mukose T (2000) Flower switching during consecutive foraging trips of Bombus ardens workers (Hymenoptera: Apidae). Entomol Sci 3:57–64Google Scholar
  57. Nicolson SW (2011) Bee food : the chemistry and nutritional value of nectar, pollen and mixtures of the two : review article. Afr Zool 46:197–204. doi: 10.3377/004.046.0201 CrossRefGoogle Scholar
  58. Nicolson SW, Thornburg RW (2007) Nectar chemistry. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and Nectar. Springer, The Netherlands, pp 215–264CrossRefGoogle Scholar
  59. Nieto A, Roberts SPM, Kemps J et al (2015) European Red list of bees. Publication Office of the European Union, LuxembourgGoogle Scholar
  60. O’Rourke AT, Fitzpatrick U, Stout JC (2014) Spring foraging resources and the behaviour of pollinating insects in fixed dune ecosystems. J Pollinat Ecol 13:161–173Google Scholar
  61. Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326. doi: 10.1111/j.1600-0706.2010.18644.x CrossRefGoogle Scholar
  62. Osborne JL, Clark SJ, Morris RJ et al (1999) A landscape-scale study of bumble bee foraging range and constancy, using harmonic radar. J Appl Ecol 36:519–533. doi: 10.1046/j.1365-2664.1999.00428.x CrossRefGoogle Scholar
  63. Patiny S, Terzo M (2010) Catalogue et clé des sous-genres et espèces du genre Andrena de Belgique et du nord de la France. Hymenoptera, ApoideaGoogle Scholar
  64. Peeters L, Totland Ø (1999) Wind to insect pollination ratios and floral traits in five alpine Salix species. Can J Bot 77:556–563. doi: 10.1139/b99-003 Google Scholar
  65. Percival MS (1961) Types of nectar in Angiosperms. New Phytol 60:235–281. doi: 10.1111/j.1469-8137.1961.tb06255.x CrossRefGoogle Scholar
  66. Persson AS, Smith HG (2013) Seasonal persistence of bumblebee populations is affected by landscape context. Agric Ecosyst Environ 165:201–209. doi: 10.1016/j.agee.2012.12.008 CrossRefGoogle Scholar
  67. Petanidou T (2005) Sugars in mediterranean floral nectars: an ecological and evolutionary approach. J Chem Ecol 31:1065–1088. doi: 10.1007/s10886-005-4248-y CrossRefPubMedGoogle Scholar
  68. Petanidou T, Ellis WN (1993) Pollinating fauna of a phryganic ecosystem: composition and diversity. Biodivers Lett 1:9–22. doi: 10.2307/2999643 CrossRefGoogle Scholar
  69. Potts SG, Vulliamy B, Dafni A et al (2003) Linking bees and flowers: how do floral communities structure pollinator communities? Ecology 84:2628–2642. doi: 10.1890/02-0136 CrossRefGoogle Scholar
  70. Prŷs-Jones OE, Corbet SA (1987) Bumblebees. The Richmond Publishing Company Ltd, SloughGoogle Scholar
  71. Rasmont P, Terzo M (2010) Catalogue et clé des sous-genres et espèces du genre Bombus de Belgique et du nord de la France (Hymenoptera, Apoidea). Université de Mons, Laboratoire de Zoologie 28 Google Scholar
  72. Rasmont P, Leclercq J, Jacob-Remacle A et al (1993) The faunistic drift of Apoidea in Belgium. In: Bruneau E (ed) Bees for pollination. Commission of the EC, Brussels, pp 65–87Google Scholar
  73. Rathcke BJ, Jules ES (1993) Habitat fragmentation and plant-pollinator interactions. Curr Sci 65:273–277Google Scholar
  74. Reille M (1992) Pollen et spores d’Europe et d’Afrique du Nord. Laboratoire de Botanique Historique et Palynologie, MarseilleGoogle Scholar
  75. Ritchie JC (1956) Vaccinium myrtillus L. J Ecol 44:291–299. doi: 10.2307/2257181 CrossRefGoogle Scholar
  76. Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209. doi: 10.1007/BF00984102 CrossRefGoogle Scholar
  77. Smeets P, Duchateau MJ (2003) Longevity of Bombus terrestris workers (Hymenoptera: Apidae) in relation to pollen availability, in the absence of foraging. Apidologie 34:333–337. doi: 10.1051/apido:2003026 CrossRefGoogle Scholar
  78. Somme L, Vanderplanck M, Michez D et al (2014) Pollen and nectar quality drive the major and minor floral choices of bumble bees. Apidologie 46:1–15. doi: 10.1007/s13592-014-0307-0 Google Scholar
  79. Stace C (2001) New flora of the British Isles. Cambridge University Press, CambridgeGoogle Scholar
  80. 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. doi: 10.1051/apido:2008017 CrossRefGoogle Scholar
  81. Terzo M, Rasmont P (2007) MALVAS, suivi, étude et vulgarisation sur l’interactionentre les MAE et les abeilles sauvages. Region Wallone direction générale de l’agriculture et université de MonsGoogle Scholar
  82. Vanderplanck M, Leroy B, Wathelet B et al (2014a) Standardized protocol to evaluate pollen polypeptides as bee food source. Apidologie 45:1–13. doi: 10.1007/s13592-013-0239-0 CrossRefGoogle Scholar
  83. Vanderplanck M, Moerman R, Rasmont P et al (2014b) How does pollen chemistry impact development and feeding behaviour of polylectic bees? PLoS ONE 9:e86209. doi: 10.1371/journal.pone.0086209 PubMedCentralCrossRefPubMedGoogle Scholar
  84. Verlinden L (1994) Faune de Belgique, Syrphides (Syrphidae). Edition de l’Institut Royal des Sciences Naturelles de Belgique, BruxellesGoogle Scholar
  85. Waddington KD, Gottlieb N (1990) Actual vs perceived profitability: a study of floral choice of honey bees. J Insect Behav 3:429–441. doi: 10.1007/BF01052010 CrossRefGoogle Scholar
  86. Waser NM, Ollerton J (2006) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, ChicagoGoogle Scholar
  87. Webb NR (1998) The traditional management of European heathlands. J Appl Ecol 35:987–990. doi: 10.1111/j.1365-2664.1998.tb00020.x CrossRefGoogle Scholar
  88. Westphal C, Steffan-Dewenter I, Tscharntke T (2006) Bumblebees experience landscapes at different spatial scales: possible implications for coexistence. Oecologia 149:289–300. doi: 10.1007/s00442-006-0448-6 CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Laura Moquet
    • 1
  • Carolin Mayer
    • 1
  • Denis Michez
    • 2
  • Bernard Wathelet
    • 3
  • Anne-Laure Jacquemart
    • 1
  1. 1.Earth and Life Institute-Research group Genetics, Reproduction, PopulationsUniversité catholique de LouvainLouvain-la-NeuveBelgium
  2. 2.Laboratory of Zoology, Institute of BiosciencesUniversity of MonsMonsBelgium
  3. 3.Industrial Biological Chemistry Unit, Gembloux Agro-Bio TechUniversity of LiègeGemblouxBelgium

Personalised recommendations