Skip to main content

Advertisement

SpringerLink
Log in

Decline of parasitic and habitat-specialist species drives taxonomic, phylogenetic and functional homogenization of sub-alpine bumblebee communities

  • Global change ecology – original research
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

The ongoing biodiversity crisis is characterised not only by an elevated extinction rate but also can lead to an increasing similarity of species assemblages. This is an issue of major concern, as it can reduce ecosystem resilience and functionality. Changes in the composition of pollinator communities have mainly been described in intensive agricultural lowland areas. In this context, using a replicated survey of historical and recent bumblebee diversity, we aimed here to test how documented changes in climate and land use influenced the potential homogenization of sub-alpine bumblebee communities in southern Norway. We assessed the change in community composition in terms of taxonomic, phylogenetic and functional (β-)diversity, and estimated the impact of various species traits in probabilities of species gains and losses. Overall, we found a strong reduction in functional diversity, but no change in phylogenetic diversity over time. The β-diversity decreased, especially at high elevations, and this pattern was consistent for taxonomic, phylogenetic and functional β-diversity. The spatial distribution, measured as the average site occupancy, decreased in habitat-specialist species. This was explained by both a higher risk of species loss and a lower probability of species gain for habitat-specialist and parasitic species than for generalist and social species. These findings demonstrate that a narrow niche breadth may contribute to a higher extinction risk in bumblebee species. This non-random impact of disturbance on species may lead to large-scale biotic homogenisation of communities, a pattern that can be detected by investigating biodiversity changes at different scales and across its multiple facets.

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
Fig. 4
Fig. 5

Similar content being viewed by others

Availability of data and materials

This manuscript reuses data from Fourcade et al (2019), available from the Figshare repository: https://doi.org/10.6084/m9.figshare.6833531.v1. All new data (e.g.: species’ traits) are available in electronic supplemental material.

References

  • Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46

    Google Scholar 

  • Baselga A (2010) Partitioning the turnover and nestedness components of beta diversity. Glob Ecol Biogeogr 19:134–143

    Article  Google Scholar 

  • Baselga A, Orme CDL (2012) betapart: an R package for the study of beta diversity. Methods Ecol Evol 3:808–812

    Article  Google Scholar 

  • Biella P, Bogliani G, Cornalba M, Manino A, Neumayer J, Porporato M, Rasmont P, Milanesi P (2017) Distribution patterns of the cold adapted bumblebee Bombus alpinus in the Alps and hints of an uphill shift (Insecta: Hymenoptera: Apidae). J Insect Conserv 21:357–366

    Article  Google Scholar 

  • Biella P, Ćetković A, Gogala A, Neumayer J, Sárospataki M, Šima P, Smetana V (2020) North-westward range expansion of the bumblebee Bombus haematurus into Central Europe is associated with warmer winters and niche conservatism. Insect Sci 28(3):861–872

    Article  PubMed  Google Scholar 

  • Bommarco R, Lundin O, Smith HG, Rundlof M (2012) Drastic historic shifts in bumble-bee community composition in Sweden. Proc R Soc B Biol Sci 279:309–315

    Article  Google Scholar 

  • Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087

    Article  Google Scholar 

  • Cameron SA, Hines HM, Williams PH (2007) A comprehensive phylogeny of the bumble bees (Bombus). Biol J Lin Soc 91:161–188

    Article  Google Scholar 

  • Ceballos G, Ehrlich PR, Barnosky AD, Garcia A, Pringle RM, Palmer TM (2015) Accelerated modern human-induced species losses: Entering the sixth mass extinction. Sci Adv 1:e1400253

    Article  PubMed  PubMed Central  Google Scholar 

  • Ceballos G, Ehrlich PR, Dirzo R (2017) Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population losses and declines. Proc Natl Acad Sci 114:E6089–E6096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen IC, Hill JK, Ohlemuller R, Roy DB, Thomas CD (2011) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026

    Article  CAS  PubMed  Google Scholar 

  • Clavel J, Julliard R, Devictor V (2011) Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ 9:222–228

    Article  Google Scholar 

  • Davies KF, Margules CR, Lawrence JF (2004) A synergistic effect puts rare, specialized species at greater risk of extinction. Ecology 85:265–271

    Article  Google Scholar 

  • De Palma A, Kuhlmann M, Bugter R, Ferrier S, Hoskins AJ, Potts SG, Roberts SPM, Schweiger O, Purvis A, Beggs J (2017) Dimensions of biodiversity loss: spatial mismatch in land-use impacts on species, functional and phylogenetic diversity of European bees. Divers Distrib 23:1435–1446

    Article  PubMed  PubMed Central  Google Scholar 

  • Devictor V, Mouillot D, Meynard C, Jiguet F, Thuiller W, Mouquet N (2010) Spatial mismatch and congruence between taxonomic, phylogenetic and functional diversity: the need for integrative conservation strategies in a changing world. Ecol Lett 13:1030–1040

    PubMed  Google Scholar 

  • Dornelas M, Gotelli NJ, McGill B, Shimadzu H, Moyes F, Sievers C, Magurran AE (2014) Assemblage time series reveal biodiversity change but not systematic loss. Science 344:296–299

    Article  CAS  PubMed  Google Scholar 

  • Dupont YL, Damgaard C, Simonsen V (2011) Quantitative historical change in bumblebee (Bombus spp.) assemblages of red clover fields. PLoS ONE 6:e25172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Elsen PR, Tingley MW (2015) Global mountain topography and the fate of montane species under climate change. Nat Climate Change 5(8):772–776

    Article  Google Scholar 

  • Faith DP (1992) Conservation evaluation and phylogenetic diversity. Biol Cons 61:1–10

    Article  Google Scholar 

  • Foufopoulos J, Ives AR (1999) Reptile extinctions on land-bridge islands: Life-history attributes and vulnerability to extinction. Am Nat 153:1–25

    Article  PubMed  Google Scholar 

  • Fourcade Y, Åström S, Öckinger E (2019) Climate and land-cover change alter bumblebee species richness and community composition in subalpine areas. Biodivers Conserv 28:639–653

    Article  Google Scholar 

  • Gagic V, Bartomeus I, Jonsson T, Taylor A, Winqvist C, Fischer C, Slade EM, Steffan-Dewenter I, Emmerson M, Potts SG, Tscharntke T, Weisser W, Bommarco R (2015) Functional identity and diversity of animals predict ecosystem functioning better than species-based indices. Proc R Soc B Biol Sci 282:20142620

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Greenleaf SS, Williams NM, Winfree R, Kremen C (2007) Bee foraging ranges and their relationship to body size. Oecologia 153:589–596

    Article  PubMed  Google Scholar 

  • Harsch MA, Hulme PE, McGlone MS, Duncan RP (2009) Are treelines advancing? A global meta-analysis of treeline response to climate warming. Ecol Lett 12:1040–1049

    Article  PubMed  Google Scholar 

  • Hoehn P, Tscharntke T, Tylianakis JM, Steffan-Dewenter I (2008) Functional group diversity of bee pollinators increases crop yield. Proc R Soc B Biol Sci 275:2283–2291

    Article  Google Scholar 

  • Hoiss B, Krauss J, Potts SG, Roberts S, Steffan-Dewenter I (2012) Altitude acts as an environmental filter on phylogenetic composition, traits and diversity in bee communities. Proc R Soc B Biol Sci 279:4447–4456

    Article  Google Scholar 

  • Jacobsen D (2020) The dilemma of altitudinal shifts: caught between high temperature and low oxygen. Front Ecol Environ 18:211–218

    Article  Google Scholar 

  • Kembel SW (2009) Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests. Ecol Lett 12:949–960

    Article  PubMed  Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR, Cornwell WK, Morlon H, Ackerly DD, Blomberg SP, Webb CO (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Kerr JT, Pindar A, Galpern P, Packer L, Potts SG, Roberts SM, Rasmont P, Schweiger O, Colla SR, Richardson LL, Wagner DL, Gall LF, Sikes DS, Pantoja A (2015) Climate change impacts on bumblebees converge across continents. Science 349:177–180

    Article  CAS  PubMed  Google Scholar 

  • Koh LP, Dunn RR, Sodhi NS, Colwell RK, Proctor HC, Smith VS (2004) Species coextinctions and the biodiversity crisis. Science 305:1632–1634

    Article  CAS  PubMed  Google Scholar 

  • Laliberte E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305

    Article  PubMed  Google Scholar 

  • Lavergne S, Mouquet N, Thuiller W, Ronce O (2010) Biodiversity and climate change: integrating evolutionary and ecological responses of species and communities. Annu Rev Ecol Evol Syst 41:321–350

    Article  Google Scholar 

  • Løken A (1973) Studies on Scandinavian bumble bees (Hymentoptera, Apidae). Norsk Entomologisk Tidsskrift 20:1–218

    Google Scholar 

  • Magurran AE, Dornelas M, Moyes F, Gotelli NJ, McGill B (2015) Rapid biotic homogenization of marine fish assemblages. Nat Commun 6:8405

    Article  CAS  PubMed  Google Scholar 

  • Marshall L, Perdijk F, Dendoncker N, Kunin W, Roberts S, Biesmeijer JC (2020) Bumblebees moving up: shifts in elevation ranges in the Pyrenees over 115 years. Proc R Soc B Biol Sci 287:20202201

    Article  Google Scholar 

  • McGill BJ, Dornelas M, Gotelli NJ, Magurran AE (2015) Fifteen forms of biodiversity trend in the Anthropocene. Trends Ecol Evol 30:104–113

    Article  PubMed  Google Scholar 

  • McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453

    Article  CAS  PubMed  Google Scholar 

  • Michonneau F, Brown JW, Winter DJ, Fitzjohn R (2016) rotl: an R package to interact with the Open Tree of Life data. Methods Ecol Evol 7:1476–1481

    Article  Google Scholar 

  • Monnet AC, Jiguet F, Meynard CN, Mouillot D, Mouquet N, Thuiller W, Devictor V (2014) Asynchrony of taxonomic, functional and phylogenetic diversity in birds. Glob Ecol Biogeogr 23:780–788

    Article  PubMed  PubMed Central  Google Scholar 

  • Mossberg B, Cederberg B (2012) Humlor i Sverige. Bonnier Fakta

  • Mouchet MA, Villéger S, Mason NWH, Mouillot D (2010) Functional diversity measures: an overview of their redundancy and their ability to discriminate community assembly rules. Funct Ecol 24:867–876

    Article  Google Scholar 

  • Müller CB, Schmid-Hempel P (1992) Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites. Ecol Entomol 17:343–353

    Article  Google Scholar 

  • Nieto A, Roberts SPM, Kemp J, Rasmont P, Kuhlmann M, García Criado M, Biesmeijer JC, Bogusch P, Dathe HH, De la Rúa 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, Tomozii B, Window J, Michez D, European Commission, Directorate-General for the Environment, and IUCN (International Union for Conservation of Nature) (2014) European red list of bees. Publications Office, Luxembourg

    Google Scholar 

  • Öckinger E, Schweiger O, Crist TO, Debinski DM, Krauss J, Kuussaari M, Petersen JD, Poyry J, Settele J, Summerville KS, Bommarco R (2010) Life-history traits predict species responses to habitat area and isolation: a cross-continental synthesis. Ecol Lett 13:969–979

    PubMed  Google Scholar 

  • Ødegaard F, Staverløkk A, Gjershaug JO, Bengtson R, Mjelde A (2015) Humler i Norge. Kjennetegn, utbredelse og levesett. Norsk institutt for naturforskning, Trondheim

    Google Scholar 

  • Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2015) vegan: community ecology package

  • Olden JD, Leroy Poff N, Douglas MR, Douglas ME, Fausch KD (2004) Ecological and evolutionary consequences of biotic homogenization. Trends Ecol Evol 19:18–24

    Article  PubMed  Google Scholar 

  • Oliver TH, Morecroft MD (2014) Interactions between climate change and land use change on biodiversity: attribution problems, risks, and opportunities. Wiley Interdiscip Rev Climate Change 5:317–335

    Article  Google Scholar 

  • Pellissier L, Pradervand J-N, Williams PH, Litsios G, Cherix D, Guisan A (2013) Phylogenetic relatedness and proboscis length contribute to structuring bumblebee communities in the extremes of abiotic and biotic gradients. Glob Ecol Biogeogr 22:577–585

    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

    Article  Google Scholar 

  • Ploquin EF, Herrera JM, Obeso JR (2013) Bumblebee community homogenization after uphill shifts in montane areas of northern Spain. Oecologia 173:1649–1660

    Article  PubMed  Google Scholar 

  • Pradervand J-N, Pellissier L, Randin CF, Guisan A (2014) Functional homogenization of bumblebee communities in alpine landscapes under projected climate change. Climate Change Responses 1:1

    Article  Google Scholar 

  • Pyke GH, Thomson JD, Inouye DW, Miller TJ (2016) Effects of climate change on phenologies and distributions of bumble bees and the plants they visit. Ecosphere 7:e01267

    Article  Google Scholar 

  • Ranta E (1982) Species structure of North European Bumblebee communities. Oikos 38:202–209

    Article  Google Scholar 

  • Rasmont P, Franzén M, Lecocq T, Harpke A, Roberts S, Biesmeijer JC, Castro L, Cederberg B, Dvorak L, Fitzpatrick Ú, Gonseth Y, Haubruge E, Mahé G, Manino A, Michez D, Neumayer J, Ødegaard F, Paukkunen J, Pawlikowski T, Potts S, Reemer M, Settele J, Straka J, Schweiger O (2015) Climatic risk and distribution atlas of European bumblebees. BioRisk 10:1–236

    Article  Google Scholar 

  • Roberts S, Potts S, Biesmeijer K, Kuhlmann M, Kunin W, Ohlemüller R (2011) Assessing continental-scale risks for generalist and specialist pollinating bee species under climate change. BioRisk 6:1–18

    Article  Google Scholar 

  • Sanders NJ, Rahbek C (2012) The patterns and causes of elevational diversity gradients. Ecography 35:1–3

    Article  Google Scholar 

  • Savage J, Vellend M (2015) Elevational shifts, biotic homogenization and time lags in vegetation change during 40 years of climate warming. Ecography 38:546–555

    Article  Google Scholar 

  • Sheffield CS, Pindar A, Packer L, Kevan PG (2013) The potential of cleptoparasitic bees as indicator taxa for assessing bee communities. Apidologie 44:501–510

    Article  Google Scholar 

  • Srivastava DS, Cadotte MW, MacDonald AA, Marushia RG, Mirotchnick N (2012) Phylogenetic diversity and the functioning of ecosystems. Ecol Lett 15:637–648

    Article  PubMed  Google Scholar 

  • van der Plas F, Manning P, Soliveres S, Allan E, Scherer-Lorenzen M, Verheyen K, Wirth C, Zavala MA, Ampoorter E, Baeten L, Barbaro L, Bauhus J, Benavides R, Benneter A, Bonal D, Bouriaud O, Bruelheide H, Bussotti F, Carnol M, Castagneyrol B, Charbonnier Y, Coomes DA, Coppi A, Bastias CC, Dawud SM, De Wandeler H, Domisch T, Finer L, Gessler A, Granier A, Grossiord C, Guyot V, Hattenschwiler S, Jactel H, Jaroszewicz B, Joly FX, Jucker T, Koricheva J, Milligan H, Mueller S, Muys B, Nguyen D, Pollastrini M, Ratcliffe S, Raulund-Rasmussen K, Selvi F, Stenlid J, Valladares F, Vesterdal L, Zielinski D, Fischer M (2016) Biotic homogenization can decrease landscape-scale forest multifunctionality. Proc Natl Acad Sci USA 113:3557–3562

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Vandewalle M, de Bello F, Berg MP, Bolger T, Dolédec S, Dubs F, Feld CK, Harrington R, Harrison PA, Lavorel S, da Silva PM, Moretti M, Niemelä J, Santos P, Sattler T, Sousa JP, Sykes MT, Vanbergen AJ, Woodcock BA (2010) Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodivers Conserv 19:2921–2947

    Article  Google Scholar 

  • Villeger S, Novack-Gottshall PM, Mouillot D (2011) The multidimensionality of the niche reveals functional diversity changes in benthic marine biotas across geological time. Ecol Lett 14:561–568

    Article  PubMed  Google Scholar 

  • Webb CO, Ackerly DD, McPeek MA, Donoghue MJ (2002) Phylogenies and community ecology. Annu Rev Ecol Syst 33:475–505

    Article  Google Scholar 

  • Williams PH, Araújo MB, Rasmont P (2007) Can vulnerability among British bumblebee (Bombus) species be explained by niche position and breadth? Biol Conserv 138:493–505

    Article  Google Scholar 

  • Winter M, Devictor V, Schweiger O (2012) Phylogenetic diversity and nature conservation: where are we? Trends Ecol Evol 28:199–204

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We thank S. Fröberg, M. Johansson, S. Larsson and M. W. Pettersson for their assistance in the field.

Funding

This study was funded by the Swedish Research Council Vetenskapsrådet, Grant Number 621-2010-5589. Y.F. was additionally funded by the Swedish Research Council FORMAS, Grant Number 2016-00667.

Author information

Authors and Affiliations

  1. Department of Ecology, Swedish University of Agricultural Sciences, Box 7044, 75007, Uppsala, Sweden

    Yoan Fourcade & Erik Öckinger

  2. Univ Paris Est Creteil, CNRS, IRD, INRAE, Sorbonne Université, Institut d’écologie et des sciences de l’environnement, IEES, 94010, Creteil, France

    Yoan Fourcade

  3. Norwegian Institute for Nature Research (NINA), Torgarden, Box 5685, 7485, Trondheim, Norway

    Sandra Åström

Authors
  1. Yoan Fourcade
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sandra Åström
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erik Öckinger
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

EÖ and SÅ conceived and designed the fieldwork, YF analysed the data and wrote the manuscript under the supervision of EÖ. All authors conceived the original ideas and contributed to the final version of the manuscript.

Corresponding author

Correspondence to Yoan Fourcade.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Ingolf Steffan-Dewenter.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 178 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fourcade, Y., Åström, S. & Öckinger, E. Decline of parasitic and habitat-specialist species drives taxonomic, phylogenetic and functional homogenization of sub-alpine bumblebee communities. Oecologia 196, 905–917 (2021). https://doi.org/10.1007/s00442-021-04970-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-021-04970-3

Keywords

Search

Navigation