Skip to main content

Advertisement

SpringerLink
Log in

Spatial and temporal variations in floral resource availability affect bumblebee communities in heathlands

  • Original Paper
  • Published:
Biodiversity and Conservation Aims and scope Submit manuscript

Abstract

Modifications of landscape structure and composition can decrease the availability of floral resources, resulting in the decline of many pollinator species, including bumblebees. These declines may have significant ecological consequences, because bumblebees pollinate a large range of plant species. Our study was carried out in heathlands, open semi-natural habitats that have decreased considerably due to human activities. We analysed how floral resources affect bumblebee communities throughout the colony lifetime at three scales: plot scale, heathland patch scale, and landscape scale. Floral density at the plot scale and spruce plantations at the landscape scale influenced bumblebee communities. The abundance of bumblebees on ericaceous species was higher when the landscape included a substantial proportion of unsuitable foraging habitat (i.e., spruce plantations). Both life history traits and colony life cycle stage influenced bumblebee responses to the availability of floral resources. Bumblebees were more affected by floral resources during the colony development phase than during the nest-foundation or mating phases. Moreover, bumblebees of species that form large colonies needed larger quantities of favourable foraging habitat, compared with small-colony bees, and their proportion decreased in habitats dominated by spruce plantations. In conclusion, the conservation of plant–bumblebee interactions will require management at a larger spatial scale than the restricted protected habitats. Moreover, at the landscape scale, both quantity of favourable foraging patches and their ecological continuity are important to conserve both small- and large- colony species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

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

    Book  Google Scholar 

  • Baillie JEM, Bennun LA, Brooks TM, Butchart SHM, Chanson JS, Cokeliss Z, Hilton-Taylor C, Hoffmann M, Mace GM, Mainka SA, Pollock CM, Rodrigues ASL, Stattersfield AJ, Stuart SN (2004) 2004 IUCN red list of threatened species: a global species assessment. IUCN, Gland

    Google Scholar 

  • Baude M, Kunin WE, Boatman ND, Conyers S, Davies N, Gillespie MAK, Morton RD, Smart SM, Memmott J (2016) Historical nectar assessment reveals the fall and rise of floral resources in Britain. Nature 530:85–88. doi:10.1038/nature16532

    Article  CAS  PubMed  PubMed Central  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 

  • Biesmeijer JC, Roberts SPM, Reemer M, Ohlemüller R, Edwards M, Peeters T, Schaffers AP, Potts SG, Kleukers R, Thomas CD (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 

  • Blüthgen N, Klein A-M (2011) Functional complementarity and specialisation: the role of biodiversity in plant–pollinator interactions. Basic Appl Ecol 12:282–291. doi:10.1016/j.baae.2010.11.001

    Article  Google Scholar 

  • Bowers MA (1985) Bumble bee colonization, extinction, and reproduction in subalpine meadows in Northeastern Utah. Ecology 66:914–927. doi:10.2307/1940554

    Article  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 

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

    Article  Google Scholar 

  • Cresswell JE, Osborne JL, Goulson D (2000) An economic model of the limits to foraging range in central place foragers with numerical solutions for bumblebees. Ecol Entomol 25:249–255. doi:10.1046/j.1365-2311.2000.00264.x

    Article  Google Scholar 

  • Decourtye A, Mader E, Desneux N (2010) Landscape enhancement of floral resources for honey bees in agro-ecosystems. Apidologie 41:264–277. doi:10.1051/apido/2010024

    Article  Google Scholar 

  • DGARNE (2014) A. Le méta-projet de restauration des tourbières de Haute-Ardenne| Projets LIFE| Agir| La biodiversité en Wallonie. In: Biodiversité En Wallonie. http://biodiversite.wallonie.be/fr/meta-projet-life-de-restauration-des-tourbieres-de-haute-ardenne.html?IDC=5778. Accessed 31 Jan 2015

  • Diaz-Forero I, Kuusemets V, Mand M, Liivamagi A, Kaart T, Luig J (2011) Effects of forest habitats on the local abundance of bumblebee species: a landscape-scale study. Balt For 17:235–242

    Google Scholar 

  • Diaz-Forero I, Kuusemets V, Mänd M, Liivamägi A, Kaart T, Luig J (2012) Influence of local and landscape factors on bumblebees in semi-natural meadows: a multiple-scale study in a forested landscape. J Insect Conserv 17:113–125. doi:10.1007/s10841-012-9490-3

    Article  Google Scholar 

  • Dreisig H (1995) Ideal free distributions of nectar foraging bumblebees. Oikos 72:161–172. doi:10.2307/3546218

    Article  Google Scholar 

  • Dunning JB, Danielson BJ, Pulliam HR (1992) Ecological processes that affect populations in complex landscapes. Oikos 65:169–175. doi:10.2307/3544901

    Article  Google Scholar 

  • Fahrig L (2001) How much habitat is enough? Biol Conserv 100:65–74. doi:10.1016/S0006-3207(00)00208-1

    Article  Google Scholar 

  • Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40:1649–1663. doi:10.1111/jbi.12130

    Article  Google Scholar 

  • Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280. doi:10.1111/j.1466-8238.2007.00287.x

    Article  Google Scholar 

  • Franzén M, Nilsson SG (2008) How can we preserve and restore species richness of pollinating insects on agricultural land? Ecography 31:698–708. doi:10.1111/j.1600-0587.2008.05110.x

    Article  Google Scholar 

  • Gascon C, Lovejoy TE, Bierregaard RO Jr, Malcolm JR, Stouffer PC, Vasconcelos HL, Laurance WF, Zimmerman B, Tocher M, Borges S (1999) Matrix habitat and species richness in tropical forest remnants. Biol Conserv 91:223–229. doi:10.1016/S0006-3207(99)00080-4

    Article  Google Scholar 

  • Goulson D (1999) Foraging strategies of insects for gathering nectar and pollen, and implications for plant ecology and evolution. Perspect Plant Ecol Evol Syst 2:185–209. doi:10.1078/1433-8319-00070

    Article  Google Scholar 

  • Goulson D (2010) Bumblebees: behaviour, ecology, and conservation. Oxford University Press, Oxford

    Book  Google Scholar 

  • Goulson D, Hanley ME, Darvill B, Ellis JS, Knight ME (2005) Causes of rarity in bumblebees. Biol Conserv 122:1–8. doi:10.1016/j.biocon.2004.06.017

    Article  Google Scholar 

  • Goulson D, Park KJ, Tinsley MC, Bussière LF, Vallejo-Marin M (2013) Social learning drives handedness in nectar-robbing bumblebees. Behav Ecol Sociobiol 67:1141–1150. doi:10.1007/s00265-013-1539-0

    Article  Google Scholar 

  • Grimmeau J-P, Decroly J, Wertz I (2013) La démographie des communes belges de 1980 à 2010. Courr Hebd CRISP 37:1–90

    Google Scholar 

  • Gustafson EJ, Gardner RH (1996) The effect of landscape heterogeneity on the probability of patch colonization. Ecology 77:94–107. doi:10.2307/2265659

    Article  Google Scholar 

  • Hatfield RG, LeBuhn G (2007) Patch and landscape factors shape community assemblage of bumble bees, Bombus spp. (Hymenoptera: Apidae), in montane meadows. Biol Conserv 139:150–158. doi:10.1016/j.biocon.2007.06.019

    Article  Google Scholar 

  • Heard MS, Carvell C, Carreck NL, Rothery P, Osborne JL, Bourke AFG (2007) Landscape context not patch size determines bumble-bee density on flower mixtures sown for agri-environment schemes. Biol Lett 3:638–641. doi:10.1098/rsbl.2007.0425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hines HM, Hendrix SD (2005) Bumble bee (Hymenoptera: Apidae) diversity and abundance in tallgrass prairie patches: effects of local and landscape floral resources. Environ Entomol 34:1477–1484. doi:10.1603/0046-225X-34.6.1477

    Article  Google Scholar 

  • Hirsch M, Pfaff S, Wolters V (2003) The influence of matrix type on flower visitors of Centaurea jacea L. Agric Ecosyst Environ 98:331–337. doi:10.1016/S0167-8809(03)00093-8

    Article  Google Scholar 

  • Irwin RE, Maloof JE (2002) Variation in nectar robbing over time, space, and species. Oecologia 133:525–533. doi:10.1007/s00442-002-1060-z

    Article  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 

  • Kremen C, Williams NM, Aizen MA, Gemmill-Herren B, LeBuhn G, Minckley R, Packer L, Potts SG, Roulston T’ai, Steffan-Dewenter I, Vázquez DP, Winfree R, Adams L, Crone EE, Greenleaf SS, Keitt TH, Klein A-M, Regetz J, Ricketts TH (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10:299–314. doi:10.1111/j.1461-0248.2007.01018.x

    Article  PubMed  Google Scholar 

  • Kreyer D, Oed A, Walther-Hellwig K, Frankl R (2004) Are forests potential landscape barriers for foraging bumblebees? Landscape scale experiments with Bombus terrestris agg. and Bombus pascuorum (Hymenoptera, Apidae). Biol Conserv 116:111–118. doi:10.1016/S0006-3207(03)00182-4

    Article  Google Scholar 

  • Kunin W, Iwasa Y (1996) Pollinator foraging strategies in mixed floral arrays: density effects and floral constancy. Theor Popul Biol 49:232–263. doi:10.1006/tpbi.1996.0013

    Article  CAS  PubMed  Google Scholar 

  • Lebuhn G, Droege S, Connor EF, Gemmill-Herren B, Potts SG, Minckley RL, Griswold T, Jean R, Kula E, Roubik DW, Cane J, Wright KW, Frankie G, Parker F (2013) Detecting insect pollinator declines on regional and global scales. Conserv Biol 27:113–120

    Article  PubMed  Google Scholar 

  • Mayer C, Michez D, Chyzy A, Brédat E, Jacquemart A-L (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  CAS  PubMed  PubMed Central  Google Scholar 

  • McFrederick QS, LeBuhn G (2006) Are urban parks refuges for bumble bees Bombus spp. (Hymenoptera: Apidae)? Biol Conserv 129:372–382. doi:10.1016/j.biocon.2005.11.004

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Moquet L, Vanderplanck M, Moerman R, Quinet M, Roger N, Michez D, Jacquemart A-L (2016) Bumblebees depend on ericaceous species to survive in temperate heathlands. Insect Conserv Divers. doi:10.1111/icad.12201

    Google Scholar 

  • Nieto A, Roberts SPM, Kemps J, Rasmont P, Kuhlmann M, García Criado M, Biesmeijer JC, Bogusch P, Dathe HH, De la Rua P, De Meulemeester T, Dehon M, Dewulf A, Ortiz-Sánchez FJ, Lhomme P, Pauly A, Potts SG, Praz C, Quaranta M, Radchenko VG, Scheuchl E, Smit J, Straka J, Terzo M, Bogdan T, Window J, Michez D (2015) European red list of bees. Publication Office of the European Union, Luxembourg

    Google Scholar 

  • Ohashi K, Yahara T (2002) Visit larger displays but probe proportionally fewer flowers: counterintuitive behaviour of nectar-collecting bumble bees achieves an ideal free distribution. Funct Ecol 16:492–503. doi:10.1046/j.1365-2435.2002.00644.x

    Article  Google Scholar 

  • Osborne JL, Clark SJ, Morris RJ, Williams IH, Riley JR, Smith AD, Reynolds DR, Edwards AS (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 

  • Pelletier L, McNeil JN (2003) The effect of food supplementation on reproductive success in bumblebee field colonies. Oikos 103:688–694. doi:10.1034/j.1600-0706.2003.12592.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 

  • Persson AS, Rundlöf M, Clough Y, Smith HG (2015) Bumble bees show trait-dependent vulnerability to landscape simplification. Biodivers Conserv 24:3469–3489. doi:10.1007/s10531-015-1008-3

    Article  Google Scholar 

  • Potts SG, Vulliamy B, Roberts S, O’Toole C, Dafni A, Ne’eman G, Willmer P (2005) Role of nesting resources in organising diverse bee communities in a Mediterranean landscape. Ecol Entomol 30:78–85. doi:10.1111/j.0307-6946.2005.00662.x

    Article  Google Scholar 

  • Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. doi:10.1016/j.tree.2010.01.007

    Article  PubMed  Google Scholar 

  • Prugh LR, Hodges KE, Sinclair ARE, Brashares JS (2008) Effect of habitat area and isolation on fragmented animal populations. Proc Natl Acad Sci 105:20770–20775. doi:10.1073/pnas.0806080105

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pyke GH, Pulliam HR, Charnov EL (1977) Optimal foraging: a selective review of theory and tests. Q Rev Biol 52:137–154

    Article  Google Scholar 

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

  • 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

    Google Scholar 

  • Rasmont P, Leclercq J, Jacob-Remacle A, Pauly A, Gaspar C (1993) The faunistic drift of Apoidea in Belgium, 65–87 In: Proceedings of an EC workshop, Bees for pollination, 2–3 March 1992, UE, Brussels, Belgium

  • Rathcke B (1983) Competition and facilitation among plants for pollination. Pollination biology. Real Leslie Academic press, London, pp 305–329

    Chapter  Google Scholar 

  • Rundlöf M, Nilsson H, Smith HG (2008) Interacting effects of farming practice and landscape context on bumble bees. Biol Conserv 141:417–426. doi:10.1016/j.biocon.2007.10.011

    Article  Google Scholar 

  • Saunders DA, Hobbs RJ, Margules CR (1991) Biological consequences of ecosystem fragmentation: a review. Conserv Biol 5:18–32

    Article  Google Scholar 

  • Somme L, Vanderplanck M, Michez D, Lombaerde I, Moerman R, Wathelet B, Wattiez R, Lognay G, Jacquemart A-L (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 

  • Steffan-Dewenter I (2003) Importance of habitat area and landscape context for species richness of bees and wasps in fragmented orchard meadows. Conserv Biol 17:1036–1044. doi:10.1046/j.1523-1739.2003.01575.x

    Article  Google Scholar 

  • Steffan-Dewenter I, Münzenberg U, Bürger C, Thies C, Tscharntke T (2002) Scale-dependent effects of landscape context on three pollinator guilds. Ecology 83:1421–1432. doi:10.2307/3071954

    Article  Google Scholar 

  • Stout JC, Allen JA, Goulson D (1998) The influence of relative plant density and floral morphological complexity on the behaviour of bumblebees. Oecologia 117:543–550

    Article  Google Scholar 

  • Suzuki Y, Kawaguchi LG, Munidasa DT, Toquenaga Y (2009) Do bumble bee queens choose nest sites to maximize foraging rate? Testing models of nest site selection. Behav Ecol Sociobiol 63:1353–1362. doi:10.1007/s00265-009-0789-3

    Article  Google Scholar 

  • Terzo M, Rasmont P (2007) MALVAS, suivi, étude et vulgarisation sur l’interaction entre les MAE et les abeilles sauvages. Région Wallonne Direction Générale de l’Agriculture et Université de Mons

  • Vaudo AD, Tooker JF, Grozinger CM, Patch HM (2015) Bee nutrition and floral resource restoration. Curr Opin Insect Sci. doi:10.1016/j.cois.2015.05.008

    Google Scholar 

  • Waddington KD (1980) Flight patterns of foraging bees relative to density of artificial flowers and distribution of nectar. Oecologia 44:199–204. doi:10.1007/BF00572680

    Article  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 

  • Williams NM, Regetz J, Kremen C (2011) Landscape-scale resources promote colony growth but not reproductive performance of bumble bees. Ecology 93:1049–1058. doi:10.1890/11-1006.1

    Article  Google Scholar 

Download references

Acknowledgements

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. Thank to Kristin Sherrard and Jennifer Mach for language improvement and the two anonymous reviewers for their valuable comments on 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”, Université catholique de Louvain) and FNRS («Fonds de la Recherche Scientifique», Web Impact Project, FRFC 2.4613.12). This research constitutes a part of L.M. Ph.D. thesis as well as the master theses for E.L. and R.B.

Author information

Author notes

  1. Rossana Bacchetta

    Present address: Centre Wallon de Recherches Agronomiques, Rue du Bordia 4, 5030, Gembloux, Belgium

  2. Estelle Laurent

    Present address: Research Group Quantitative Conservation Biology, Earth and Life Institute – Université catholique de Louvain, Croix du Sud 4-5, Box L7.07.04, Louvain-la-Neuve, Belgium

Authors and Affiliations

  1. Research Group Genetics, Reproduction, Populations, Earth and Life Institute – Université catholique de Louvain, Croix du Sud 2, Box L7.05.14, 1348, Louvain-la-Neuve, Belgium

    Laura Moquet, Rossana Bacchetta, Estelle Laurent & Anne-Laure Jacquemart

Authors
  1. Laura Moquet
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rossana Bacchetta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Estelle Laurent
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Anne-Laure Jacquemart
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura Moquet.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by B. D. Hoffmann.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Moquet, L., Bacchetta, R., Laurent, E. et al. Spatial and temporal variations in floral resource availability affect bumblebee communities in heathlands. Biodivers Conserv 26, 687–702 (2017). https://doi.org/10.1007/s10531-016-1266-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10531-016-1266-8

Keywords

Search

Navigation