Abstract
Widespread alterations in species distribution and abundance as a result of global environmental change include upwards and polewards shifts driven by local extinctions in the south or at lower elevations and colonizations of newly available habitat elements in the north or at higher elevations. Although cumulative changes on patterns of community composition are also expected, studies following a community-level approach are still scarce. Here, we estimate changes in abundance and distribution of bumblebee (Bombus spp.) species over two decades along an elevational gradient to test whether these changes entailed concomitant alterations on patterns of community composition. Bumblebee species showed an overall trend to shift uphill their upper- or lower-elevational boundaries, resulting in narrower elevational ranges from one period to another, coincident with a regional warming of ca. 0.9 °C. Changes in elevational ranges were, however, mainly related to retractions of the lower limit of species distribution, rather than to variations in their upper elevational limit. Species turnover was associated with colonization and extinction events and also with variability in the relative abundance of short-, medium- and long-tongued species along the elevational gradient. Extinctions were especially relevant at medium elevations, while only communities at higher elevations had a positive net outcome between colonization and extinction events. The combination of these effects resulted in the homogenization of bumblebee assemblages, especially between medium and upper elevations. The changes reported in our study strongly match with predictions of global change driving elevational shifts in species distribution and provide the first evidence of elevational changes in bumblebees at both species and community level.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Álvarez MA, de Castro M, Cruz R, Gómez A, Pérez V, Stöll H (2009) Clima. In: Consejería de Medio Ambiente, Ordenación del Territorio en Infraestructuras (eds) Evidencias y efectos potenciales del cambio climático en Asturias. Gobierno del Principado de Asturias, Oviedo, pp 56–67
Angert AL, Crozier LG, Rissler LJ, Gilman SE, Tewksbury JJ, Chunco AJ (2011) Do species’ traits predict recent shifts at expanding range edges? Ecol Lett 14:677–689. doi:10.1111/j.1461-0248.2011.01620.x
Bingham RA, Orthner AR (1998) Efficient pollination of alpine plants. Nature 391:238–239. doi:10.1038/34564
Bommarco R, Lundin O, Smith HG, Rundlöf M (2011) Drastic historic shifts in bumble-bee community composition in Sweden. Proc R Soc B 279:309–315. doi:10.1098/rspb.2011.0647
Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci USA 108:662–667. doi:10.1073/pnas.1014743108
Chen I-C, Hill JK, Ohlemüller R, Roy DB, Thomas CD (2011a) Rapid range shifts of species associated with high levels of climate warming. Science 333:1024–1026. doi:10.1126/science.1206432
Chen IC, et al. (2011b) Asymmetric boundary shifts of tropical montane Lepidoptera over four decades of climate warming. Glob Ecol Biogeogr 20:34–45. doi:10.1111/j.1466-8238.2010.00594.x
Clavel J, Julliard R, Devictor V (2011) Worldwide decline of specialist species: toward a global functional homogenization? Front Ecol Environ 9:222–228. doi:10.1890/080216
Devictor V, van Swaay C, Brereton T, Brotons L, Chamberlain D, Heliölä J, Herrando S, Julliard R, Kuussaari M, Lindström A, Reif J, Roy DB, Schweiger O, Settele J, Stefanescu C, Van Strien A, Van Turnhout C, Vermouzek Z, WallisDeVries M, Wynhoff I, Jiguet F (2012) Differences in the climatic debts of birds and butterflies at a continental scale. Nat Clim Change 2:121–124. doi:10.1038/nclimate1347
Díaz TE, Fernández JA (1987) Asturias y Cantabria. In: Peinado M, Rivas-Martínez S (eds) La vegetación de España. Universidad de Alcalá de Henares, Madrid, pp 77–116
Dupont YL, Damgaard C, Simonsen V (2011) Quantitative historical change in bumblebee (Bombus spp.) assemblages of red clover fields. PLoS ONE 6:e25172. doi:10.1371/journal.pone.0025172
Franco AM, Hill JK, Kitschke C, Collingham YC, Roy DB, Fox R, Huntley B, Thomas CD (2006) Impacts of climate warming and habitat loss on extinctions at species’ low-latitude range boundaries. Glob Change Biol 12:1545–1553. doi:10.1111/j.1365-2486.2006.01180.x
Franzén M, Öckinger E (2012) Climate-driven changes in pollinator assemblages during the last 60 years in an Arctic mountain region in Northern Scandinavia. J Insect Conserv 16:227–238. doi:10.1007/s10841-011-9410-y
García D, Quevedo M, Obeso JR, Abajo A (2005) Fragmentation patterns and protection of montane forest in the Cantabrian range (NW Spain). For Ecol Manage 208:29–43. doi:10.1016/j.foreco.2004.10.071
González-Megías A, Menendez R, Roy D, Brereton T, Thomas CD (2008) Changes in the composition of British butterfly assemblages over two decades. Glob Change Biol 14:1464–1474. doi:10.1111/j.1365-2486.2008.01592.x
Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391. doi:10.1046/j.1461-0248.2001.00230.x
Goulson D, Darvill B (2004) Niche overlap and diet breadth in bumblebees; are rare species more specialized in their choice of flowers? Apidologie 35:55–63. doi:10.1051/apido:2003062
Goulson D, Hanley M, Darvill B, Ellis J, Knight M (2005) Causes of rarity in bumblebees. Biol Conserv 122:1–8. doi:10.1016/j.biocon.2004.06.017
Goulson D, Lye GC, Darvill B (2008) Diet breadth, coexistence and rarity in bumblebees. Biodivers Conserv 17:3269–3288. doi:10.1007/s10531-008-9428-y
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
Hagen M, Wikelski M, Kissling WD (2011) Space use of bumblebees (Bombus spp.) revealed by radio-tracking. PLoS ONE 6:e19997. doi:10.1371/journal.pone.0019997
Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:184–195. doi:10.1111/j.1461-0248.2008.01269.x
Heinrich B (1979) Bumblebee economics. Harvard University Press, Cambridge
Hickling R, Roy DB, Hill JK, Fox R, Thomas CD (2006) The distributions of a wide range of taxonomic groups are expanding polewards. Glob Change Biol 12:450–455. doi:10.1111/j.1365-2486.2006.01116.x
Hill MO, Gauch HG (1980) Detrended correspondence analysis: an improved ordination technique. Plant Ecol 42:47–58. doi:10.1007/BF00048870
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 279:4447–4456. doi:10.1098/rspb.2012.1581
IPCC (Intergovernmental Panel on Climate Change) (2007) Climate change 2007: the physical science basis. Cambridge University Press, Cambridge
Jiguet F, Gadot AS, Julliard R, Newson SE, Couvet D (2007) Climate envelope, life history traits and the resilience of birds facing global change. Glob Change Biol 13:1672–1684. doi:10.1111/j.1365-2486.2007.01386.x
Kindt R, Coe R (2005) Tree diversity analysis. A manual and software for common statistical methods for ecological and biodiversity studies. World Agroforestry Centre (ICRAF), Nairobi
Kosior A, 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
Legendre P, Legendre L (1998) Numerical ecology, 2nd edn. Elsevier, Amsterdam
Lenoir J, Gégout JC, Marquet PA, De Ruffray P, Brisse H (2008) A significant upward shift in plant species optimum elevation during the 20th century. Science 320:1768–1771. doi:10.1126/science.1156831
Macdonald M (2001) The colonisation of Northern Scotland by Bombus terrestris (L.) and B. lapidarius (L.) (Hym., Apidae), and the possible role of climate change. Entomol Mon Mag 137:1–14
McKinney ML, Lockwood JL (1999) Biotic homogenization: a few winners replacing many losers in the next mass extinction. Trends Ecol Evol 14:450–453. doi:10.1016/j.bbr.2011.03.031
MMA-DGB (2005) 2º Inventario Forestal Nacional. Ministerio de Medio Ambiente, Dirección General de la Biodiversidad. Base de Datos de la Biodiversidad, Madrid
Nakagawa S, Cuthill IC (2007) Effect size, confidence interval and statistical significance: a practical guide for biologists. Biol Rev 82:591–605. doi:10.1111/j.1469-185X.2007.00027.x
Obeso JR (1992) Geographic distribution and community structure of bumblebees in the northern Iberian peninsula. Oecologia 89:244–252. doi:10.1007/BF00317224
Oksanen J et al. (2011) Vegan: community ecology package. R package version 2.0–3
Olden JD (2006) Biotic homogenization: a new research agenda for conservation biogeography. J Biogeogr 33:2027–2039. doi:10.1111/j.1365-2699.2006.01572.x
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. doi:10.1146/annurev.ecolsys.37.091305.110100
Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42. doi:10.1038/nature01286
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
Pyke GH (1982) Local geographic distributions of bumblebees near Crested Butte, Colorado: competition and community structure. Ecology 63:555–573. doi:10.2307/1938970
R Development Core Team (2011) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Rasmont P, Iserbyt I (2010) Atlas of the European bees: genus Bombus. 2nd edn. STEP project, atlas Hymenoptera, Mons, Gembloux. http://www.zoologie.umh.ac.be//hymenoptera/page.asp?ID=169
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Ricketts TH, Regetz J, Steffan-Dewenter I, Cunningham SA, Kremen C, Bogdanski A, Gemmill-Herren B, Greenleaf SS, Klein AM, Mayfield MM, Morandin LA, Ochieng A, Viana BF (2008) Landscape effects on crop pollination services: are there general patterns? Ecol Lett 11:499–515. doi:10.1111/j.1461-0248.2008.01157.x
Shaffer HB, Fisher RN, Davidson C (1998) The role of natural history collections in documenting species declines. Trends Ecol Evol 13:27–30. doi:10.1016/S0169-5347(97)01177-4
Sheldon KS, Yang S, Tewksbury JJ (2011) Climate change and community disassembly: impacts of warming on tropical and temperate montane community structure. Ecol Lett 14:1191–1200. doi:10.1111/j.1461-0248.2011.01689.x
Stefanescu C, Carnicer J, Penuelas J (2011) Determinants of species richness in generalist and specialist Mediterranean butterflies: the negative synergistic forces of climate and habitat change. Ecography 34:353–363. doi:10.1111/j.1600-0587.2010.06264.x
Tingley MW, Monahan WB, Beissinger SR, Moritz C (2009) Birds track their Grinnellian niche through a century of climate change. Proc Nat Acad Sci USA 106:19637–19643. doi:10.1073/pnas.0901562106
Warren MS, Hill JK, Thomas JA, Asher J, Fox R, Huntley B, Roy DB, Telfer MG, Jeffcoate S, Harding P, Jeffcoate G, Willis SG, Greatorex-Davies JN, Moss D, Thomas CD (2001) Rapid responses of British butterflies to opposing forces of climate and habitat change. Nature 414:65–69. doi:10.1038/35102054
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. doi:10.1016/j.biocon.2007.06.001
Williams PH, Colla SR, XIE ZH (2009) Bumblebee vulnerability: common correlates of winners and losers across three continents. Conserv Biol 23:931–940. doi:10.1111/j.1523-1739.2009.01176.x
Wilson RJ, Gutiérrez D, Gutiérrez J, Martínez D, Agudo R, Monserrat VJ (2005) Changes to the elevational limits and extent of species ranges associated with climate change. Ecol Lett 8:1138–1146. doi:10.1111/j.1461-0248.2005.00824.x
Wilson RJ, Gutiérrez D, Gutiérrez J, Monserrat VJ (2007) An elevational shift in butterfly species richness and composition accompanying recent climate change. Glob Change Biol 13:1873–1887. doi:10.1111/j.1365-2486.2007.01418.x
Acknowledgments
We would like to thank Amalia Segura for helping in the field. Comments by Javier Rodríguez-Pérez and two anonymous reviewers greatly improved the manuscript. Ronnie Lendrum edited the English style. Funding was provided by the Regional Government of Asturias and the Spanish Government with the BP08-047 fellowship (Foundation for Promotion in Asturias of Applied and Technological Scientific Research, FICYT) to E. F. P. and the CGL2009-11302 grant (Science and Innovation Ministry, MICCIN) to J. R. O.
Conflict of interest
The authors declare that they have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Ingolf Steffan-Dewenter.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ploquin, E.F., Herrera, J.M. & Obeso, J.R. Bumblebee community homogenization after uphill shifts in montane areas of northern Spain. Oecologia 173, 1649–1660 (2013). https://doi.org/10.1007/s00442-013-2731-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-013-2731-7