Skip to main content
SpringerLink
Log in

Fruit orchards and woody semi-natural habitat provide complementary resources for pollinators in agricultural landscapes

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Context

To safeguard insect pollinators and their pollination services, we need to understand how landscape structure regulates the distribution of resources that sustain pollinator populations. However, evidence of how pollinator communities benefit from the variety of resources distributed across different habitat types is scarce.

Objectives

To explore complementary resource provision, we conducted a field study to examine the resources available to pollinators in fruit orchards and woody semi-natural habitat.

Methods

We studied 13 landscapes containing both habitat types in Flanders, Belgium. In every habitat element, we surveyed nesting resources, floral resources and wild pollinators (i.e. wild bees and hover flies) during three consecutive time periods in the season (once before- and twice after mass-flowering of the fruit orchards).

Results

We concluded that the composition of nesting resources for wild bees was clearly different between both habitat types. Woody semi-natural habitat also provided more diverse- and a higher cover of floral resources compared to fruit orchards. In addition, the composition of these floral resources became more and more distinct between the two habitat types as the season progressed. Based on the plant − pollinator network we identified key plant species for inclusion in management schemes to support pollinators.

Conclusions

Our study highlights that fruit orchards and woody semi-natural habitat provide a set of different, complementary resources during the flight season, for pollinating insects. Due to the higher diversity and abundance of resources in woody semi-natural habitat, conservation of woody semi-natural habitat is essential for the support of pollinators in agricultural landscapes.

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

Data availability

Data is available from the Dryad Digital Repository https://doi.org/10.5061/dryad.44j0zpcbh

References

  • Anderson MJ, Walsh DCI (2013) PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: What null hypothesis are you testing? Ecol Monogr 83:557–574

    Article  Google Scholar 

  • Baldock KCR, Goddard MA, Hicks DM et al (2019) A systems approach reveals urban pollinator hotspots and conservation opportunities. Nat Ecol Evol 3:363–373

    Article  PubMed  PubMed Central  Google Scholar 

  • Balfour NJ, Ollerton J, Castellanos MC, Ratnieks FLW (2018) British phenological records indicate high diversity and extinction rates among late-summer-flying pollinators. Biol Conserv 222:278–283

    Article  Google Scholar 

  • Batáry P, Gallé R, Riesch F et al (2017) The former Iron Curtain still drives biodiversity-profit trade-offs in German agriculture. Nat Ecol Evol 1:1279–1284

    Article  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B and Walker S (2019) lme4: Linear mixed-effects models using Eigen and S4. R Package Version 1.1-21. https://cran.r-project.org/web/packages/lme4/lme4.pdf. Accessed 30 Dec 2020

  • Bertrand C, Eckerter PW, Ammann L et al (2019) Seasonal shifts and complementary use of pollen sources by two bees, a lacewing and a ladybeetle species in European agricultural landscapes. J Appl Ecol 56:2431–2442

    Article  Google Scholar 

  • Buckles BJ, Harmon-Threatt AN (2019) Bee diversity in tallgrass prairies affected by management and its effects on above- and below-ground resources. J Appl Ecol 56:2443–2453

    Article  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

    Article  PubMed  PubMed Central  Google Scholar 

  • Dainese M, Montecchiari S, Sitzia T et al (2017) High cover of hedgerows in the landscape supports multiple ecosystem services in Mediterranean cereal fields. J Appl Ecol 54:380–388

    Article  Google Scholar 

  • Dainese M, Martin EA, Aizen MA et al (2019) A global synthesis reveals biodiversity-mediated benefits for crop production. Sci Adv 5(eaax0121):16

    Google Scholar 

  • De Cáceres M, Legendre P, Moretti M (2010) Improving indicator species analysis by combining groups of sites. Oikos 119:1674–1684

    Article  Google Scholar 

  • De Saeger S and K Scheers (2016) The Biological Valuation Map of the Flemish Research Institute for Nature and Forest (INBO). https://www.inbo.be/en/inbobiological-valuation-map. Accessed 12 Feb 2020

  • Dormann CF, Fruend J and Gruber B (2020) Package ‘bipartite’. R Package Version 2.15. https://cran.r-project.org/web/packages/bipartite/bipartite.pdf. Accessed 6 April 2020

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

    Article  Google Scholar 

  • Eeraerts M, Meeus I, Van Den Berge S, Smagghe G (2017) Landscapes with high intensive fruit cultivation reduce wild pollinator services to sweet cherry. Agric Ecosyst Environ 239:342–348

    Article  Google Scholar 

  • Eeraerts M, Smagghe G, Meeus I (2019) Pollinator diversity, floral resources and semi-natural habitat, instead of honey bees and intensive agriculture, enhance pollination service to sweet cherry. Agric Ecosyst Environ 284:106586

    Article  Google Scholar 

  • Fahrig L, Baudry J, Brotons L et al (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112

    Article  PubMed  Google Scholar 

  • Foley JA, DeFries R, Asner GP et al (2005) Global consequences of land use. Science (-80) 309:570–574

    Article  CAS  Google Scholar 

  • Garibaldi LA, Steffan-Dewenter I, Winfree R et al (2013) Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339:1608–1611

    Article  CAS  PubMed  Google Scholar 

  • Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347:1–16

    Article  Google Scholar 

  • Hartig F (2019) DHARMa: Residual diagnostics for hierarchical (multi-level/mixed) regression models. R package version 0.2.6. https://cran.r-project.org/web/packages/DHARMa/vignettes/DHARMa.html. Accessed 30 Dec 2019

  • Hass AL, Kormann UG, Tscharntke T et al (2018) Landscape configurational heterogeneity by small-scale agriculture, not crop diversity, maintains pollinators and plant reproduction in western Europe. Proc R Soc B 285:20172242

    Article  PubMed  Google Scholar 

  • Hennekens S (2009) Protocol ‘Vegetatieopname.’ Wageningen, Alterra, p 12

    Google Scholar 

  • Kells AR, Goulson D (2003) Preferred nesting sites of bumblebee queens (Hymenoptera: Apidae) in agroecosystems in the UK. Biol Conserv 109:165–174

    Article  Google Scholar 

  • Kennedy CM, Lonsdorf E, Neel MC et al (2013) A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecol Lett 16:584–599

    Article  PubMed  Google Scholar 

  • Kleijn D, Winfree R, Bartomeus I et al (2015) Delivery of crop pollination services is an insufficient argument for wild pollinator conservation. Nat Commun 6:1–8

    Article  Google Scholar 

  • Mallinger RE, Gibbs J, Gratton C (2016) Diverse landscapes have a higher abundance and species richness of spring wild bees by providing complementary floral resources over bees’ foraging periods. Landsc Ecol 31:1523–1535

    Article  Google Scholar 

  • Mandelik Y, Winfree R, Neeson T, Kremen C (2012) Complementary habitat use by wild bees in agro-natural landscapes. Ecol Appl 22:1535–1546

    Article  PubMed  Google Scholar 

  • Martin EA, Dainese M, Clough Y et al (2019) The interplay of landscape composition and configuration: new pathways to manage functional biodiversity and agroecosystem services across Europe. Ecol Lett 22:1083–1094

    Article  PubMed  Google Scholar 

  • Martins KT, Albert CH, Lechowicz MJ, Gonzalez A (2018) Complementary crops and landscape features sustain wild bee communities. Ecol Appl 28:1093–1105

    Article  PubMed  Google Scholar 

  • O’connor S, Park KJ, Goulson D (2017) Location of bumblebee nests is predicted by counts of nest-searching queens. Ecol Entomol 42:731–736

    Article  Google Scholar 

  • Öckinger E, Smith HG (2007) Semi-natural grasslands as population sources for pollinating insects in agricultural landscapes. J Appl Ecol 44:50–59

    Article  Google Scholar 

  • Oksanen J, Blanchet FG, Friendly M, et al (2019) Vegan: Community ecology package. R package Version 2.5-6. https://cran.r-project.org/web/packages/vegan/vegan.pdf. Accessed 30 Dec 2019

  • Ollerton J, Erenler H, Edwards M, Crockett R (2014) Extinctions of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science 346:1360–1362

    Article  CAS  PubMed  Google Scholar 

  • Park MG, Blitzer EJ, Gibbs J et al (2015) Negative effects of pesticides on wild bee communities can be buffered by landscape context. Proc R Soc B Biol Sci 282:20150299

    Article  Google Scholar 

  • Pinheiro J and Bates D (2019) nlme: Linear and Nonlinear Mixed Effects Models. R package Version 3.1-143. https://cran.r-project.org/web/packages/nlme/nlme.pdf. Accessed 30 Dec 2019

  • Potts SG, Vulliamy B, Roberts S et al (2005) Role of nesting resources in organising diverse bee communities in a Mediterranean landscape. Ecol Entomol 30:78–85

    Article  Google Scholar 

  • Powney GD, Carvell C, Edwards M et al (2019) Widespread losses of pollinating insects in Britain. Nat Commun 10:1018

    Article  PubMed  PubMed Central  Google Scholar 

  • Proesmans W, Smagghe G, Meeus I et al (2019) The effect of mass-flowering orchards and semi-natural habitat on bumblebee colony performance. Landsc Ecol 34:1033–1044

    Article  Google Scholar 

  • Proesmans W (2019) The importance of small forest fragments for pollination services in agricultural landscapes. PhD Thesis. Ghent University, Belgium

  • Purvis EEN, Meehan ML, Lindo Z (2020) Agricultural field margins provide food and nesting resources to bumble bees (Bombus spp., Hymenoptera: Apidae) in Southwestern Ontario, Canada. Insect Conserv Divers 13:219–228

    Article  Google Scholar 

  • QGIS Development Team (2018) QGIS Geographic Information System. Open Source Geospatial Foundation Project.

  • R Development Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rader R, Cunningham SA, Howlett BG, Inouye DW (2020) Non-bee insects as visitors and pollinators of crops: biology, ecology and management. Annu Rev Entomol 65:1–17

    Article  Google Scholar 

  • Requier F, Leonhardt SD (2020) Beyond flowers: including non-floral resources in bee conservation schemes. J Insect Conserv 24:5–16

    Article  Google Scholar 

  • Roulston TH, Goodell K (2011) The role of resources and risks in regulating wild bee populations. Annu Rev Entomol 56:293–312

    Article  CAS  PubMed  Google Scholar 

  • Sardiñas HS, Kremen C (2014) Evaluating nesting microhabitat for ground-nesting bees using emergence traps. Basic Appl Ecol 15:161–168

    Article  Google Scholar 

  • Scheper J, Holzschuh A, Kuussaari M et al (2013) Environmental factors driving the effectiveness of European agri-environmental measures in mitigating pollinator loss—a meta-analysis. Ecol Lett 16:912–920

    Article  PubMed  Google Scholar 

  • Scheper J, Reemer M, Van Kats R et al (2014) Museum specimens reveal loss of pollen host plants as key factor driving wild bee decline in the Netherlands. Proc Natl Acad Sci USA 111:17552–17557

    Article  CAS  PubMed  Google Scholar 

  • Science for Environment Policy (2017) Agri-environmental schemes: how to enhance the agriculture-environment relationship. Thematic Issue 57. Issue produced for the European Commission DG Environment by the Science Communication Unit, UWE, Bristol. Available at: Retrieved on 8 January 2020 from http://ec.europa.eu/science-environmentpolicy

  • Senapathi D, Carvalheiro LG, Biesmeijer JC et al (2015) The impact of over 80 years of land cover changes on bee and wasp pollinator communities in England. Proc R Soc B 282:20150294

    Article  PubMed  Google Scholar 

  • Sirami C, Gross N, Baillod AB et al (2019) Increasing crop heterogeneity enhances multitrophic diversity across agricultural regions. Proc Natl Acad Sci USA 116:16442–16447

    Article  CAS  PubMed  Google Scholar 

  • Steffan-Dewenter I, Tscharntke T (2000) Resource overlap and possible competition between honey bees and wild bees in central Europe. Oecologia 122:288–296

    Article  CAS  PubMed  Google Scholar 

  • Steffan-Dewenter I, Schiele S (2008) Do resources or natural enemies drive bee population dynamics in fragmented habitats? Ecology 89:1375–1387

    Article  PubMed  Google Scholar 

  • Sutter L, Jeanneret P, Bartual AM et al (2017) Enhancing plant diversity in agricultural landscapes promotes both rare bees and dominant crop-pollinating bees through complementary increase in key floral resources. J Appl Ecol 54:1856–1864

    Article  Google Scholar 

  • Timberlake TP, Vaughan IP, Memmott J (2019) Phenology of farmland floral resources reveals seasonal gaps in nectar availability for bumblebees. J Appl Ecol 56:1585–1596

    Article  Google Scholar 

  • Tscharntke T, Klein AM, Kruess A et al (2005) Landscape perspectives on agricultural intensification and biodiversity—ecosystem service management. Ecol Lett 8:857–874

    Article  Google Scholar 

  • Tscharntke T, Tylianakis JM, Rand TA et al (2012) Landscape moderation of biodiversity patterns and processes - eight hypotheses. Biol Rev 87:661–685

    Article  PubMed  Google Scholar 

  • Van Den Berge S, Baeten L, Vanhellemont M et al (2018) Species diversity, pollinator resource value and edibility potential of woody networks in the countryside in northern Belgium. Agric Ecosyst Environ 259:119–126

    Article  Google Scholar 

  • Van Den Berge S, Tessens S, Baeten L et al (2019) Contrasting vegetation change (1974–2015) in hedgerows and forests in an intensively used agricultural landscape. Appl Veg Sci 22:269–281

    Article  Google Scholar 

  • Williams NM, Kremen C (2007) Resource distributions among habitats determine solitary bee offspring production in a mosaic landscape. Ecol Appl 17:910–921

    Article  PubMed  Google Scholar 

  • Winfree R, Bartomeus I, Cariveau DP (2011) Native pollinators in anthropogenic habitats. Annu Rev Ecol Evol Syst 42:1–22

    Article  Google Scholar 

  • Wood TJ, Holland JM, Goulson D (2015) Pollinator-friendly management does not increase the diversity of farmland bees and wasps. Biol Conserv 187:120–126

    Article  Google Scholar 

Download references

Acknowledgement

The authors declare no conflict of interest. ME was funded by the Research Foundation Flanders PhD grant 1S71416N. We gratefully acknowledge Delphine Parmentier, Anne-Sophie Sacré, Veerle Stro and Lieve Van Lysebettens for their assistance in the field. We also thank the farmers for providing access to their orchards, and Jonathan Willow for his useful comments and linguistic review of the manuscript.

Author information

Authors and Affiliations

  1. Agrozoology Lab, Department of Plant and Crops, Ghent University, Coupure Links 653, Ghent, 9000, Belgium

    Maxime Eeraerts, Guy Smagghe & Ivan Meeus

  2. Forest & Nature Lab, Department of Environment, Ghent University, Geraardsbergsesteenweg 267, Melle-Gontrode, 9090, Belgium

    Sanne Van Den Berge & Kris Verheyen

  3. Natuurpunt Studie, Coxiestraat 11, Mechelen, 2800, Belgium

    Willem Proesmans

Authors
  1. Maxime Eeraerts
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sanne Van Den Berge
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Willem Proesmans
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kris Verheyen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Guy Smagghe
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ivan Meeus
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Maxime Eeraerts.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Electronic supplementary material 1 (DOCX 1734 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Eeraerts, M., Van Den Berge, S., Proesmans, W. et al. Fruit orchards and woody semi-natural habitat provide complementary resources for pollinators in agricultural landscapes. Landscape Ecol 36, 1377–1390 (2021). https://doi.org/10.1007/s10980-021-01220-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-021-01220-y

Keywords

Search

Navigation