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

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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.

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References

  • Aerts R, Heil GW (1993) Heathlands: patterns and processes in a changing environment. Kluwer Academic Publishers, Dordrecht

    Book  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 117–141

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Benton T (2006) Bumblebees: the natural history and identification of the species found in Britain. Collins, London

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

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

    Google Scholar 

  • Buchmann SL, Nabhan GP (1997) The Forgotten Pollinators. Island Press, Washington (DC)

    Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Clicheroux E (1957) L’évolution des terrains incultes en Belgique. Bull Inst Rech Économiques Soc 23:497–524

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • De Groot AP (1953) Protein and amino acid requirements of the honeybee (Apis mellifica L.). Physiol Comp Oecol 3:1–90

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

  • Development Core Team R (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. doi:10.2307/30033784

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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, Germany

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Gimingham CH (1972) Ecology of Heathlands. Chapman & Hall, London

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Harder LD (1985) Morphology as a predictor of flower choice by bumble bees. Ecology 66:198–210. doi:10.2307/1941320

    Article  Google Scholar 

  • 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 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Inouye DW (1978) Resource partitioning in bumblebees: experimental studies of foraging behavior. Ecology 59:672–678. doi:10.2307/1938769

    Article  Google Scholar 

  • Jacquemart AL (1992) Préliminaires sur la production de nectar chez trois espèces de Vaccinium. Apidologie 23:453–464. doi:10.1051/apido:19920507

    Article  Google Scholar 

  • Jacquemart A-L (1993) Floral visitors of Vaccinium species in the high Ardenne, Belgium. Flora 188:263–273

    Google Scholar 

  • 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 

  • 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 95:345–351

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Katoh N, Goto N, Iizumi S (1985) Sugar composition of nectar in flowers of Salix species. Sci Rep Res Inst Tohoku Univ 39:45–52

    Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Lack AJ (1982) The ecology of flowers of chalk grassland and their insect pollinators. J Ecol 70:773–790. doi:10.2307/2260104

    Article  Google Scholar 

  • 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, Meise

    Google Scholar 

  • 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 69:185–194

    Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  Google Scholar 

  • Morse DH (1977) Resource partitioning in bumble bees: the role of behavioral factors. Science 197:678–680. doi:10.1126/science.197.4304.678

    Article  CAS  PubMed  Google Scholar 

  • Nagamitsu T, Yoneda M, Mukose T (2000) Flower switching during consecutive foraging trips of Bombus ardens workers (Hymenoptera: Apidae). Entomol Sci 3:57–64

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Nicolson SW, Thornburg RW (2007) Nectar chemistry. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and Nectar. Springer, The Netherlands, pp 215–264

    Chapter  Google Scholar 

  • Nieto A, Roberts SPM, Kemps J et al (2015) European Red list of bees. Publication Office of the European Union, Luxembourg

    Google Scholar 

  • O’Rourke AT, Fitzpatrick U, Stout JC (2014) Spring foraging resources and the behaviour of pollinating insects in fixed dune ecosystems. J Pollinat Ecol 13:161–173

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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, Apoidea

    Google Scholar 

  • 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 

  • Percival MS (1961) Types of nectar in Angiosperms. New Phytol 60:235–281. doi:10.1111/j.1469-8137.1961.tb06255.x

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Petanidou T, Ellis WN (1993) Pollinating fauna of a phryganic ecosystem: composition and diversity. Biodivers Lett 1:9–22. doi:10.2307/2999643

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Prŷs-Jones OE, Corbet SA (1987) Bumblebees. The Richmond Publishing Company Ltd, Slough

    Google Scholar 

  • 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 

  • 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 65–87

  • Rathcke BJ, Jules ES (1993) Habitat fragmentation and plant-pollinator interactions. Curr Sci 65:273–277

    Google Scholar 

  • Reille M (1992) Pollen et spores d’Europe et d’Afrique du Nord. Laboratoire de Botanique Historique et Palynologie, Marseille

    Google Scholar 

  • Ritchie JC (1956) Vaccinium myrtillus L. J Ecol 44:291–299. doi:10.2307/2257181

    Article  Google Scholar 

  • Roulston TH, Cane JH (2000) Pollen nutritional content and digestibility for animals. Plant Syst Evol 222:187–209. doi:10.1007/BF00984102

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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 

  • Stace C (2001) New flora of the British Isles. Cambridge University Press, Cambridge

    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. doi:10.1051/apido:2008017

    Article  CAS  Google Scholar 

  • 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 Mons

  • 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

    Article  Google Scholar 

  • 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

    Article  PubMed Central  PubMed  Google Scholar 

  • Verlinden L (1994) Faune de Belgique, Syrphides (Syrphidae). Edition de l’Institut Royal des Sciences Naturelles de Belgique, Bruxelles

    Google Scholar 

  • 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

    Article  Google Scholar 

  • Waser NM, Ollerton J (2006) Plant-pollinator interactions: from specialization to generalization. University of Chicago Press, Chicago

    Google Scholar 

  • Webb NR (1998) The traditional management of European heathlands. J Appl Ecol 35:987–990. doi:10.1111/j.1365-2664.1998.tb00020.x

    Article  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

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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).

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Table 5 Bumblebee OTU composition adapted for Belgium (operational taxonomic units, from Terzo and Rasmont 2007)

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Moquet, L., Mayer, C., Michez, D. et al. Early spring floral foraging resources for pollinators in wet heathlands in Belgium. J Insect Conserv 19, 837–848 (2015). https://doi.org/10.1007/s10841-015-9802-5

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