Folia Geobotanica

, Volume 51, Issue 2, pp 143–159 | Cite as

Plant functional traits – fixed facts or variable depending on the season?

  • Christine Römermann
  • Solveig Franziska Bucher
  • Melanie Hahn
  • Markus Bernhardt-Römermann
Article

Abstract

Traits are widely used to detect and explain responses of ecosystem processes to environmental changes. Various studies use trait data from databases, often providing one value per trait and species, neglecting intraspecific trait variability along spatio-temporal gradients. Handbooks for standardized trait measurements claim that traits should be measured at an ‘optimal’ stage, which is typically defined to be reached when the plants are in full blossom. However, it is unclear whether this method is appropriate. The main aim of this study was to quantify the extent to which trait values vary with season and phenology, a type of variation that has been overlooked so far relative to other sources of intraspecific variation. Further, we aimed to investigate whether species rankings remain consistent throughout the year.

From April to November 2012, we monitored seven leaf traits [specific leaf area SLA, leaf dry matter content, chlorophyll fluorescence parameters (Fv/Fm, performance-index PI], stomatal density, stomatal size and the stomatal pore area index SPI) of 15 summer green woody species weekly under controlled conditions. In parallel, we recorded phenological stages.

The results showed that all traits varied significantly throughout the year in a species-specific manner. We detected trait relationships with vegetative but not with flowering phenology. Species rankings were inconsistent throughout the season in all traits.

We concluded that the seasonal timing of trait measurements is crucial. Most notably SLA, Fv/Fm and stomatal size were the most robust traits in terms of small intraspecific and large interspecific variation and showed largely consistent species rankings across seasons.

Keywords

Fv/Fm intraspecific trait variability LDMC phenology SLA stomatal density 

Supplementary material

12224_2016_9250_MOESM1_ESM.docx (930 kb)
ESM 1(DOCX 930 kb)

References

  1. Al Haj Khaled R, Duru M, Theau JP, Plantureux S, Cruz P (2005) Variation in leaf traits through seasons and N-availability levels and its consequences for ranking grassland species. J Veg Sci 16:391–398CrossRefGoogle Scholar
  2. Albert CH, Thuiller W, Yoccoz NG, Douzet R, Aubert S, Lavorel S (2010) A multi-trait approach reveals the structure and the relative importance of intra- vs interspecific variability in plant traits. Funct Ecol 24:1192–1201CrossRefGoogle Scholar
  3. Bernhardt-Römermann M, Römermann C, Sperlich S, Schmidt W (2011a) Explaining grassland biomass – the contribution of climate, species and functional diversity depends on fertilisation and mowing frequency. J Appl Ecol 48:1088–1097CrossRefGoogle Scholar
  4. Bernhardt-Römermann M, Gray A, Vanbergen AJ, Berges L, Bohner A, Brooker RW, De Bruyn L, De Cinti B, Dirnbock T, Grandin U, Hester AJ, Kanka R, Klotz S, Loucougaray G, Lundin L, Matteucci G, Meszaros I, Viktor O, Preda E, Prevosto B, Pykala J, Schmidt W, Taylor ME, Vadineanu A, Waldmann T, Stadler J (2011b) Functional traits and local environment predict vegetation responses to disturbance: a pan-European multi-site experiment. J Ecol 99:777–787CrossRefGoogle Scholar
  5. Bucher SF, Auerswald K, Tautenhahn S, Geiger A, Otto JCS, Müller A, Römermann C (2016) Inter- and intraspecific variation in stomatal pore area index along elevational gradients and its relation to leaf functional traits. Pl Ecol 217:229–240CrossRefGoogle Scholar
  6. Carlson JE, Adams CA, Holsinger KE (2016) Intraspecific variation in stomatal traits, leaf traits and physiology reflects adaptation along aridity gradients in a South African shrub. Ann Bot 117:195–207CrossRefPubMedGoogle Scholar
  7. Casson S, Gray JE (2008) Influence of environmental factors on stomatal development. New Phytol 178:9–23CrossRefPubMedGoogle Scholar
  8. Clark AJ, Landolt W, Bucher J, Strasser R (2000) Beech (Fagus sylvatica) response to ozone exposure assessed with a chlorophyll a fluorescence performance index. Environm Pollut 109:501–507CrossRefGoogle Scholar
  9. Cornelissen JHC, Lavorel S, Garnier E, Diaz S, Buchmann N, Gurvich DE, Reich PB, ter Steege H, Morgan HD, van der Heijden MGA, Pausas JG (2003) Handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust J Bot 51:335–380CrossRefGoogle Scholar
  10. Craine JM, Froehle J, Tilman DG, Wedin DA, Chapin FS (2001) The relationships among root and leaf traits of 76 grassland species and relative abundance along fertility and disturbance gradients. Oikos 93:274–285CrossRefGoogle Scholar
  11. Crawley MJ (2007) The R Book. Ed. 1, John Wiley & SonsGoogle Scholar
  12. de Bello F, Lavorel S, Albert CH, Thuiller W, Grigulis K, Dolezal J, Janecek S, Leps J (2011) Quantifying the relevance of intraspecific trait variability for functional diversity Meth Ecol Evol 2:163–174CrossRefGoogle Scholar
  13. Dias M, Brüggemann W (2010) Limitations of photosynthesis in Phaseolus vulgaris under drought stress: gas exchange, chlorophyll fluorescence and Calvin cycle enzymes. Photosynthetica 48:96–102CrossRefGoogle Scholar
  14. Dierschke H (1972) Zur Aufnahme und Darstellung phänologischer Erscheinungen in Pflanzengesellschaften. In Van der Maarel ET , Tüxen R (eds) Grundfragen und Methoden in der Pflanzensoziologie. Springer, Den Haag, pp 291–311CrossRefGoogle Scholar
  15. Dubey P, Raghubanshi AS, Singh JS (2011) Intra-seasonal variation and relationship among leaf traits of different forest herbs in a dry tropical environment. Curr Sci 100:69–76Google Scholar
  16. Franks PJ, Leitch IJ, Ruszala EM, Hetherington AM, Beerling DJ (2012) Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations. Philos Trans, Ser B 367:537–546CrossRefGoogle Scholar
  17. Garnier E, Laurent G, Bellmann A, Debain S, Berthelier P, Ducout B, Roumet C, Navas ML (2001) Consistency of species ranking based on functional leaf traits. New Phytol 152:69–83CrossRefGoogle Scholar
  18. Gay AP, Hurd RG (1975) The Influence of Light on Stomatal Density in the Tomato. New Phytol 1:37–46CrossRefGoogle Scholar
  19. Grant, B. W. & Vatnick, I. (2004) Environmental Correlates of Leaf Stomata Density. Teaching issues and Experiments in Ecology, 1, 1–24Google Scholar
  20. Griffin KL, Epstein DJ, Boelman NT (2013) Hill Slope Variations in Chlorophyll Fluorescence Indices and Leaf Traits in a Small Arctic Watershed. Arctic Antarct Alpine Res 45:39–49CrossRefGoogle Scholar
  21. Hilu K, Randall J (1984) Convenient method for studying grass leaf epidermis. Taxon 33:413–415CrossRefGoogle Scholar
  22. Holland N, Richardson AD (2009) Stomatal Length Correlates with Elevation of Growth in Four Temperate Species. J Sustain Forest 28:63–73CrossRefGoogle Scholar
  23. Holland V, Koller S, Brüggemann W (2014) Insight into the photosynthetic apparatus in evergreen and deciduous European oaks during autumn senescence using OJIP fluorescence transient analysis. Pl Biol 16:801–808CrossRefGoogle Scholar
  24. Hulshof CM, Swenson NG (2010) Variation in leaf functional trait values within and across individuals and species: an example from a Costa Rican dry forest. Funct Ecol 24:17–223CrossRefGoogle Scholar
  25. Hulshof CM, Violle C, Spasojevic MJ, McGill B, Damschen E, Harrison S, Enquist BJ (2013) Intra-specific and inter-specific variation in specific leaf area reveal the importance of abiotic and biotic drivers of species diversity across elevation and latitude. J Veg Sci 24:921–931CrossRefGoogle Scholar
  26. Jurik TW (1986a) Seasonal patterns of leaf photosynthetic capacity in successional northern hardwood tree species. Amer J Bot 73:131–138CrossRefGoogle Scholar
  27. Jurik TW (1986b) Temporal and spatial patterns of specific leaf weight in successional northern hardwood tree species. Amer J Bot 73:1083–1092CrossRefGoogle Scholar
  28. Kahmen S, Poschlod P (2004) Plant functional trait responses to grassland succession over 25 years. J Veg Sci 15:21–32CrossRefGoogle Scholar
  29. Karavin N, Kilinc M (2011) Variation in SLA and LMA of Deciduous Quercus cerris var cerris and Evergreeen Phillyrea latifolia According to Directional, Seasonal and Climatical Parameters. Ekoloji 20:21–29CrossRefGoogle Scholar
  30. Kattge J, Diaz 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, Fernandez-Mendez 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, Llusia 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, Ordonez J, Overbeck G, Ozinga WA, Patino S, Paula S, Pausas JG, Penuelas 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 JF, 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. Global Change Biol 17:2905–2935CrossRefGoogle Scholar
  31. Kazakou E, Violle C, Roumet C, Navas M L, Vile D, Kattge J, and Garnier E (2014) Are trait-based species rankings consistent across data sets and spatial scales? J Veg Sci 25:235–247CrossRefGoogle Scholar
  32. Kikuzawa K, Lechowicz MJ (2011) Ecology of Leaf Longevity. Ed. 1, Springer JapanGoogle Scholar
  33. Kleyer M, Bekker RM, Knevel IC, Bakker JP, Thompson K, Sonnenschein M, Poschlod P, Van Groenendal JM, Klimes L, Klimesova J, Klotz S, Rusch G, Hermy M, Adriaens D, Boedeltje G, Bossuyt B, Endels P, Götzenberger L, Hodgson JG, Jackel A-K, Dannemann,A, Kühn I, Kunzmann D, Ozinga W, Römermann C, Stadler M, Schlegelmilch J, Steendam H, Tackenberg O, Wilmann B, Cornelissen JHC, Eriksson O, Garnier E, Fitter A, Peco B (2008) The LEDA traitbase, A database of plant life-history traits of North West Europe. J Ecol 96:1266–1274Google Scholar
  34. Knevel IC, Bekker RM, Bakker JP, Kleyer M (2003) Life-history traits of the Northwest European Flora: the LEDA database J Veg Sci 14:611–614CrossRefGoogle Scholar
  35. Lauterbach D, Römermann C, Jeltsch F, Ristow M (2013) Factors driving plant rarity in dry grasslands on different spatial scales: a functional trait approach. Biodiv & Conservation 22:2337–2352Google Scholar
  36. Lavorel S, Rochette C, Lebreton JD (1999) Functional groups for response to disturbance in Mediterranean old fields. Oikos 84:480–498CrossRefGoogle Scholar
  37. Muggeo VMR (2003) Estimating regression models with unknown break-points. Statist Med 22:3055–3071CrossRefGoogle Scholar
  38. Muggeo VMR (2008) segmented: an R Package to Fit Regression Models with Broken-Line Relationships. R News 8:20–25Google Scholar
  39. Palacio S, Milla R, Albuixech J, Perez-Rontome C, Camarero JJ, Maestro M, Montserrat-Marti G (2008) Seasonal variability of dry matter content and its relationship with shoot growth and nonstructural carbohydrates. New Phytol 180:133–142CrossRefPubMedGoogle Scholar
  40. Perez-Harguindeguy N, Diaz S, Garnier E, Lavorel S, Poorter H, Jaureguiberry P, Bret-Harte M S, Cornwell W K, Craine J M, Gurvich D E, Urcelay C, Veneklaas E J, Reich P B, Poorter L, Wright I J, Ray P, Enrico L, Pausas J G, de Vos A C, Buchmann N, Funes G, Quetier F, Hodgson J G, Thompson K, Morgan H D, ter Steege H, van der Heijden M G A, Sack L, Blonder B, Poschlod P, Vaieretti M V, Conti G, Staver A C, Aquino S & Cornelissen J H C (2013) New handbook for standardised measurement of plant functional traits worldwide. Austral J Bot 61:167–234Google Scholar
  41. Poole I, Weyers JDB, Lawson T, Raven JA (1996) Variations in stomatal density and index: implications for palaeoclimatic reconstructions. Pl Cell Environm 19:705–712CrossRefGoogle Scholar
  42. R Foundation for Statistical Computing (2014) R: A language and environment for statistical computing ViennaGoogle Scholar
  43. Rizopoulos D (2006) ltm: An R package for latent variable modelling and item response theory analyses. J Statist Softw 17:1–25CrossRefGoogle Scholar
  44. Roche P, Díaz-Burlinson N, Gachet, S (2004) Congruency analysis of species ranking based on leaf traits: which traits are the more reliable? Pl Ecol 174:37–48CrossRefGoogle Scholar
  45. Römermann C, Bernhardt-Römermann M, Kleyer M, Poschlod P (2009) Substitutes for grazing in semi-natural grasslands- do mowing or mulching represent valuable alternatives to maintain vegetation structure? J Veg Sci 20:1086–1098CrossRefGoogle Scholar
  46. Sack L, Cowan PD, Jaikumar N, Holbrook NM (2003) The 'hydrology' of leaves: co-ordination of structure and function in temperate woody species. Pl Cell Environm 26:1343–1356CrossRefGoogle Scholar
  47. Schreiber U, Bilger W, Neubauer C (1995) Chlorophyll fluorescence as a nonintrusive indicator for rapid assessment of in vivo photosynthesis. In: Ecophysiology of photosynthesis. Springer, pp 49–70Google Scholar
  48. Steer BT (1971) Dynamics of leaf growth and photosynthetic capacity in Capsicum frutescens L.. Ann Bot 35:1003–1015Google Scholar
  49. Stojnic S, Orlovic S, Miljkovic D, Galic Z, Kebert M, von Wuehlisch G (2015) Provenance plasticity of European beech leaf traits under differing environmental conditions at two Serbian common garden sites. Eur J Forest Res 134:1109–1125CrossRefGoogle Scholar
  50. Strasser RJ, Srivastava A, Tsimilli-Michael M (1999) Screening the vitality and photosynthetic activity of plants by fluorescence transient. In Behl RK, Punia MS, Lather BPS (eds) Crop improvement for food security, Hisar, SSARM, pp 79–126Google Scholar
  51. Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. In Yunus M, Pathre U, Mohanty P (eds) Probing photosynthesis: mechanisms, regulation and adaptation. Taylor and Francis, London, pp 443–480Google Scholar
  52. Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the Chlorophyll a fluorescence transient. In Papageorgiou GC , Govindjee (eds) Chlorophyll fluorescence: A signature of photosynthesis. Kluwer, Dordrecht, pp 321–362CrossRefGoogle Scholar
  53. Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme Plant Soil 199:213–227CrossRefGoogle Scholar
  54. White AJ, Critchley C (1999) Rapid light curves: A new fluorescence method to assess the state of the photosynthetic apparatus. Photosyn Res 59:63–72CrossRefGoogle Scholar
  55. Wisskirchen R, Haeupler H (1998) Standardliste der Farn- und Blütenpflanzen Deutschlands. (Ed. 1), Ulmer, Stuttgart (Hohenheim)Google Scholar
  56. Woodward F, Lake J, Quick W (2002) Stomatal development and CO2: ecological consequences. New Phytol 153:477–484CrossRefGoogle Scholar
  57. Wright IJ, Reich PB, Cornelissen JHC, Falster DS, Groom PK, Hikosaka K, Lee W, Lusk CH, Niinemets U, Oleksyn J, Osada N, Poorter H, Warton DI, Westoby M (2005) Modulation of leaf economic traits and trait relationships by climate. Global Ecol Biogeogr 14:411–421CrossRefGoogle Scholar
  58. Zeileis A (2004) Econometric Computing with HC and HAC Covariance Matrix Estimators. J Statist Softw 11:1–17CrossRefGoogle Scholar
  59. Zeileis A, Hothorn T (2002) Diagnostic Checking in Regression Relationships. R News 2:7–10Google Scholar

Copyright information

© Institute of Botany, Academy of Sciences of the Czech Republic 2016

Authors and Affiliations

  • Christine Römermann
    • 1
    • 2
  • Solveig Franziska Bucher
    • 1
  • Melanie Hahn
    • 3
  • Markus Bernhardt-Römermann
    • 4
  1. 1.Plant Biodiversity Group, Institute of Systematic BotanyFriedrich-Schiller University JenaJenaGermany
  2. 2.German Centre for Integrative Biodiversity Research (iDiv)Halle-Jena-LeipzigLeipzigGermany
  3. 3.Theoretical Ecology, Institute of BotanyRegensburg UniversityRegensburgGermany
  4. 4.Institute of EcologyFriedrich-Schiller University JenaJenaGermany

Personalised recommendations