Abstract
Snowbed habitats are home to plant species that have adapted to particular environmental conditions (i.e. long-lasting snow cover and short growing seasons). The presence of most of these species is dependent on a long period of snow cover and so their conservation may well depend in the future on their ability to adapt to the effects of climate change. The aim of this study was to assess the persistence of snowbed communities using functional trait and functional diversity indices. We used data for plant species abundances from 32 snowbeds in Andorra (Pyrenees) classified according to certain environmental variables (elevation, exposure, soil type and temperature) and snow cover duration. Nine functional traits were used to evaluate the functional diversity, which was characterised as consisting of functional richness, functional evenness, functional dispersion, functional divergence and the community-weighted mean trait values. In two snowbeds, plant traits were also recorded and variation analysed along a snowmelt gradient. We found that snowbed specialist species had functional traits that were well adapted to the particular abiotic conditions of snowbed habitats but that there was a predominance of the functional traits of grass species in species originating in neighbouring communities. We found less functional richness, fewer strategies and lower competitive ability in the adapted species as the severity of the abiotic conditions increased. Snowbed specialist species appear to be less sensitive to the length of the growing season than species from neighbouring communities. Our results suggest that non-specialist species will tend to appear more frequently in those snowbed habitats affected by the reduction in snow cover duration.
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References
ACIA (2005) Arctic climate impact assessment: scientific report. Cambridge University Press, Cambridge
Apostolova II, Pedashenko H, Sopotlieva D, Velev N, Vassilev K, Meshinev T (2013) Arctic-Alpine plants in Bulgarian mountains. Lazaroa 34:55–63. doi:10.5209/rev_LAZA.2013.v34.n1.43180
Baptist F, Flahaut C, Streb P, Choler P (2010) No increase in alpine snowbed productivity in response to experimental lengthening of the growing season. Plant Biol 12:755–764. doi:10.1111/j.1438-8677.2009.00286.x
Billings WD, Mooney HA (1968) The ecology of arctic and alpine plants. Biol Rev 43:481–529. doi:10.1111/j.1469-185X.1968.tb00968.x
Björk R, Molau U (2007) Ecology of alpine snowbeds and the impact of global change. Arct Antarct Alp Res 39:34–43
Botta-Dukát Z (2005) Rao’s quadratic entropy as a measure of functional diversity based on multiple traits. J Veg Sci 16:533–540
Choler P (2005) Consistent shifts in alpine plant traits along a mesotopographical gradient. Arct Antarct Alp Res 37:444–453
Cornelissen JHC, Lavorel S, Garnier E, Díaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG, Poorter H (2003) A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380
Cornwell WK, Schwilk DW, Ackerly DD (2006) A trait-based test for habitat filtering: convex hull volume. Ecology 87:1465–1471
Crawley MJ (2007) The R Book. Wiley, West Sussex
Currie DJ, Mittelbach GG, Cornell HV, Field R, Guégan J-F, Hawkins BA, Kaufman DM, Kerr JT, Oberdorff T, O’Brien E, Turner JRG (2004) Predictions and tests of climate-based hypotheses of broad-scale variation in taxonomic richness. Ecol Lett 7:1121–1134. doi:10.1111/j.1461-0248.2004.00671.x
De Bello F, Lavorel S, Lavergne S, Albert CH, Boulangeat I, Mazel F, Thuiller W (2012) Hierarchical effects of environmental filters on the functional structure of plant communities: a case study in the French Alps. Ecography 36:393–402
De Bolòs O, Vigo J, Masalles RM, Ninot JM (2005) Flora manual dels països catalans, 3rd edn. Portic, Barcelona
Domènech M (2012) Cartografia de les congestes i ecologia de les comunitats vegetals de les congestes d’Andorra (Pirineus). Universitat de Lleida, Lleida
Domènech M, Conesa JA, Peñuelas J, Komac B (2014) Site-specific factors influence the richness and phenology of snowbed plants in the Pyrenees. Plant Biosyst. doi:10.1080/11263504.2014.990941
Dubuis A, Rossier L, Pottier J, Pellissier L, Vittoz P, Guisan A (2013) Predicting current and future spatial community patterns of plant functional traits. Ecography 36:1158–1168. doi:10.1111/j.1600-0587.2013.00237.x
Dullinger S, Mang T, Dirnböck T, Ertl S, Gattringer A, Grabherr G, Leitner M, Hülber K (2011) Patch configuration affects alpine plant distribution. Ecography 34:576–587. doi:10.1111/j.1600-0587.2010.06601.x
Fernández Calzado MR, Molero Mesa J (2011) High altitude flora of Sierra Nevada (Spain). Flora Mediterr 21:247–259
Flynn DF, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, Simpson N, Mayfield MM, DeClerck F (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12:22–33
Friedman J, Harder LD (2004) Inflorescence architecture and wind pollination in six grass species. Funct Ecol 18:851–860. doi:10.1111/j.0269-8463.2004.00921.x
Garnier E, Cortez J, Billès G, Navas M-L, Roumet C, Debussche M, Laurent G, Blanchard A, Aubry D, Bellmann A, Neill C, Toussaint J-P (2004) Plant functional markers capture ecosystem properties during secondary succession. Ecology 85:2630–2637. doi:10.1890/03-0799
Geertsema W, Opdam P, Kropff M (2002) Plant strategies and agricultural landscapes: survival in spatially and temporally fragmented habitat. Landsc Ecol 17:263–279
Grabherr G (2003) Alpine vegetation dynamics and climate change - A synthesis of long-term studies and observations. In: Nagy L, Grabherr G, Körner C, Thompson DB (eds) Alpine Biodiversity in Europe. Springer, Berlin, pp 399–409
Grace JB, Harrison S, Damschen EI (2011) Local richness along gradients in the Siskiyou herb flora: R. H. Whittaker revisited. Ecology 92:108–120. doi:10.1890/09-2137.1
Grime JP (2001) Plant Strategies, Vegetation Processes, and Ecosystem Properties. Wiley, Chichester
Heegaard E, Vandvik V (2004) Climate change affects the outcome of competitive interactions: an application of principal response curves. Oecologia 139:459–466. doi:10.1007/s00442-004-1523-5
Hodgson JG, Wilson PJ, Hunt R, Grime JP, Thompson K (1999) Allocating C–S–R plant functional types: a soft approach to a hard problem. Oikos 85:282–294
Hodkinson ID (2005) Terrestrial insects along elevation gradients: species and community responses to altitude. Biol Rev 80:489–513. doi:10.1017/S1464793105006767
Huelber K, Gottfried M, Pauli H, Reiter K, Winkler M, Grabherr G (2006) Phenological responses of snowbed species to snow removal dates in the Central Alps: implications for climate warming. Arct Antarct Alp Res 38:99–103
Hultén E, Fries M (1986) Atlas of north European vascular plants. Koeltz Scientific Books, Königstein
Kattge J, Díaz S, Lavorel S, Prentice IC, Leadley P, Bönisch G, Garnier E, Westoby M, Reich PB, Wright IJ, Cornelissen JHC, Violle C, Harrison SP, Van Bodegom PM, Reichstein M, Enquist BJ, Soudzilovskaia NA, Ackerly DD, Anand M, Atkin O, Bahn M, Baker TR, Baldocchi D, Bekker R, Blanco CC, Blonder B, Bond WJ, Bradstock R, Bunker DE, Casanoves F, Cavender-Bares J, Chambers JQ, Chapin Iii FS, Chave J, Coomes D, Cornwell WK, Craine JM, Dobrin BH, Duarte L, Durka W, Elser J, Esser G, Estiarte M, Fagan WF, Fang J, Fernández-Méndez F, Fidelis A, Finegan B, Flores O, Ford H, Frank D, Freschet GT, Fyllas NM, Gallagher RV, Green WA, Gutierrez AG, Hickler T, Higgins SI, Hodgson JG, Jalili A, Jansen S, Joly CA, Kerkhoff AJ, Kirkup D, Kitajima K, Kleyer M, Klotz S, Knops JMH, Kramer K, Kühn I, Kurokawa H, Laughlin D, Lee TD, Leishman M, Lens F, Lenz T, Lewis SL, Lloyd J, Llusià J, Louault F, Ma S, Mahecha MD, Manning P, Massad T, Medlyn BE, Messier J, Moles AT, Müller SC, Nadrowski K, Naeem S, Niinemets Ü, Nöllert S, Nüske A, Ogaya R, Oleksyn J, Onipchenko VG, Onoda Y, Ordoñez J, Overbeck G, Ozinga WA, Patiño S, Paula S, Pausas JG, Peñuelas J, Phillips OL, Pillar V, Poorter H, Poorter L, Poschlod P, Prinzing A, Proulx R, Rammig A, Reinsch S, Reu B, Sack L, Salgado-Negret B, Sardans J, Shiodera S, Shipley B, Siefert A, Sosinski E, Soussana J-F, Swaine E, Swenson N, Thompson K, Thornton P, Waldram M, Weiher E, White M, White S, Wright SJ, Yguel B, Zaehle S, Zanne AE, Wirth C (2011) TRY: a global database of plant traits. Glob Chang Biol 17:2905–2935. doi:10.1111/j.1365-2486.2011.02451.x
Komac B, Domènech M, Fanlo R (2014) Effects of grazing on plant species diversity and pasture quality in subalpine grasslands in the eastern Pyrenees (Andorra): Implications for conservation. J Nat Conserv 22:247–255. doi:10.1016/j.jnc.2014.01.005
Körner C (2003) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer, Ney York
Kudo G, Hirao AS (2006) Habitat-specific responses in the flowering phenology and seed set of alpine plants to climate variation: implications for global-change impacts. Popul Ecol 48:49–58. doi:10.1007/s10144-005-0242-z
Kudo G, Suzuki S (1999) Flowering phenology of alpine plant communities along a gradient of snowmelt timing. Polar Biosci 12:100–113
Laliberté E, Legendre P (2010) A distance-based framework for measuring functional diversity from multiple traits. Ecology 91:299–305
Laliberté E, Shipley B (2011) FD: Measuring functional diversity (FD) from multiple traits, and other tools for functional ecology. Austria, Vienna
Lesica P, McCune B (2004) Decline of arctic-alpine plants at the southern margin of their range following a decade of climatic warming. J Veg Sci 15:679–690. doi:10.1111/j.1654-1103.2004.tb02310.x
Lluent A (2007) Estudi de l’estructura i funcionament de les comunitats quionòfiles als Pirineus en relació a la variació dels factors ambientals. Barcelona University (UB)
Lluent A, Anadon-Rosell A, Ninot JM, Grau O, Carrillo E (2013) Phenology and seed setting success of snowbed plant species in contrasting snowmelt regimes in the Central Pyrenees. Flora Morphol Distrib Funct Ecol Plants 208:220–231. doi:10.1016/j.flora.2013.03.004
López-Moreno JI, Goyette S, Beniston M (2009) Impact of climate change on snowpack in the Pyrenees: horizontal spatial variability and vertical gradients. J Hydrol 374:384–396. doi:10.1016/j.jhydrol.2009.06.049
Mason NWH, Mouillot D, Lee WG, Wilson JB (2005) Functional richness, functional evenness and functional divergence: the primary components of functional diversity. Oikos 111:112–118. doi:10.1111/j.0030-1299.2005.13886.x
Mason NWH, Irz P, Lanoiselée C, Mouillot D, Argillier C (2008) Evidence that niche specialization explains species–energy relationships in lake fish communities. J Anim Ecol 77:285–296. doi:10.1111/j.1365-2656.2007.01350.x
Mason NWH, de Bello F, Mouillot D, Pavoine S, Dray S (2013) A guide for using functional diversity indices to reveal changes in assembly processes along ecological gradients. J Veg Sci 24:794–806. doi:10.1111/jvs.12013
Mokany K, Ash J, Roxburgh S (2008) Functional identity is more important than diversity in influencing ecosystem processes in a temperate native grassland. J Ecol 96:884–893. doi:10.1111/j.1365-2745.2008.01395.x
Molau U (1997) Phenology and reproductive success in arctic plants: susceptibility to climate change. In: Oechel WC, Callaghan TV, Gilmanov TG, Holten JI, Maxwell B, Molau U, Sveinbjörnsson B (eds) Global change and arctic terrestrial ecosystems. Springer, New York, pp 153–170
Molau U, Nordenhäll U, Eriksen B (2005) Onset of flowering and climate variability in an alpine landscape: a 10-year study from Swedish Lapland. Am J Bot 92:422–431. doi:10.3732/ajb.92.3.422
Mouchet MA, Villeger 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
Nagy L (2006) European high mountain (Alpine) vegetation and its suitability for indicating climate change impacts. Biol Environ Proc R Ir Acad 106:335–341. doi:10.3318/BIOE.2006.106.3.335
Nagy L, Grabherr G (2009) The biology of alpine habitats. Oxford University Press, New York
Ninot JM, Grau O, Carrillo E, Guàrdia R, Lluent A, Illa E (2013) Functional plant traits and species assemblage in Pyrenean snowbeds. Folia Geobot 48:23–38. doi:10.1007/s12224-012-9138-9
Økland RH (1999) On the variation explained by ordination and constrained ordination axes. J Veg Sci 10:131–136. doi:10.2307/3237168
Pakeman RJ (2012) Functional diversity indices reveal the impacts of land use intensification on plant community assembly. J Ecol 99:1143–1151
Pakeman RJ (2014) Leaf dry matter content predicts herbivore productivity, but Its functional diversity is positively related to resilience in grasslands. PLoS ONE 9:e101876. doi:10.1371/journal.pone.0101876
Pakeman RJ, Lennon JJ, Brooker RW (2011) Trait assembly in plant assemblages and its modulation by productivity and disturbance. Oecologia 167:209–218. doi:10.1007/s00442-011-1980-6
Rao RC (1964) The use and interpretation of principal component analysis in applied research. Indian J Stat Ser A, 329–358
Rivas-Martínez S, Fernández-González F, Loidi J, Lousã M, Penas Á (2002) Syntaxonomical checklist of vascular plant communities of Spain and Portugal to association level. Itinera Geobot 14:5–341
Scherrer D, Körner C (2011) Topographically controlled thermal-habitat differentiation buffers alpine plant diversity against climate warming. J Biogeogr 38:406–416. doi:10.1111/j.1365-2699.2010.02407.x
Schöb C, Kammer P, Kikvidze Z, Choler P, Veit H (2008) Changes in species composition in alpine snowbeds with climate change inferred from small-scale spatial patterns. Web Ecol 8:142–159
Schöb C, Kammer PM, Choler P, Veit H (2009) Small-scale plant species distribution in snowbeds and its sensitivity to climate change. Plant Ecol 200:91–104. doi:10.1007/s11258-008-9435-9
Schönswetter P, Paun O, Tribsch A, Niklfeld H (2003) Out of the Alps: colonization of northern Europe by east alpine populations of the glacier buttercup Ranunculus glacialis L. (Ranunculaceae). Mol Ecol 12:3373–3381. doi:10.1046/j.1365-294X.2003.01984.x
Shimono Y, Kudo G (2003) Intraspecific variations in seedling emergence and survival of Potentilla matsumurae (Rosaceae) between alpine fellfield and snowbed habitats. Ann Bot 91:21–29. doi:10.1093/aob/mcg002
Spasojevic MJ, Suding KN (2011) Inferring community assembly mechanisms from functional diversity patterns: the importance of multiple assembly processes. J Ecol 100:652–661
Spasojevic MJ, Grace JB, Harrison S, Damschen EI (2014) Functional diversity supports the physiological tolerance hypothesis for plant species richness along climatic gradients. J Ecol 102:447–455. doi:10.1111/1365-2745.12204
Stöcklin J, Kuss P, Pluess AR (2009) Genetic diversity, phenotypic variation and local adaptation in the alpine landscape: case studies with alpine plant species. Bot Helvetica 119:125–133. doi:10.1007/s00035-009-0065-1
Tomaselli M (1991) The snow-bed vegetation in the Northern Apennines. Vegetatio 94:177–189. doi:10.1007/BF00032630
Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301. doi:10.1890/07-1206.1
Virtanen R (2000) Effects of grazing on above-ground biomass on a mountain snowbed, NW Finland. Oikos 90:295–300. doi:10.1034/j.1600-0706.2000.900209.x
Westoby M, Falster DS, Moles AT, Vesk PA, Wright IJ (2002) Plant ecological strategies: some leading dimensions of variation between species. Annu Rev Ecol Syst 33:125–159
Wipf S (2010) Phenology, growth, and fecundity of eight subarctic tundra species in response to snowmelt manipulations. Plant Ecol 207:53–66. doi:10.1007/s11258-009-9653-9
Wipf S, Rixen C, Mulder CPH (2006) Advanced snowmelt causes shift towards positive neighbour interactions in a subarctic tundra community. Glob Change Biol 12:1496–1506. doi:10.1111/j.1365-2486.2006.01185.x
Wipf S, Stoeckli V, Bebi P (2009) Winter climate change in alpine tundra: plant responses to changes in snow depth and snowmelt timing. Clim Change 94:105–121. doi:10.1007/s10584-009-9546-x
Yoshie F (2008) Dormancy of alpine and subalpine perennial forbs. Ecol Res 23:35–40. doi:10.1007/s11284-007-0334-7
Acknowledgments
The authors are grateful to Michael Lockwood for the linguistic corrections. The authors were funded by Spanish Government grant CGL2010-17172/BOS, Catalan Government grant SGR 2009-458 and European Government Synergy-ERC grant 610028 IMBALANCE-P. The study was supported by the TRY initiative on plant traits (http://www.trydb.org). The TRY initiative and database is hosted, developed and maintained by J. Kattge and G. Bönisch (Max-Planck-Institute for Biogeochemistry, Jena, Germany). TRY is supported by DIVERSITAS, IGBP, the Global Land Project, the UK Natural Environment Research Council (NERC) via its program QUEST (Quantifying and Understanding the Earth System), the French Foundation for Biodiversity Research (FRB) and GIS “Climat, Environnement et Société” France.
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Komac, B., Pladevall, C., Peñuelas, J. et al. Variations in functional diversity in snowbed plant communities determining snowbed continuity. Plant Ecol 216, 1257–1274 (2015). https://doi.org/10.1007/s11258-015-0506-4
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DOI: https://doi.org/10.1007/s11258-015-0506-4