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Functional traits of grasses growing in open and shaded habitats

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Abstract

The amount of light available for photosynthesis is a key environmental factor that shapes the form and function of plants. Several plant traits affect the manner in which different species fix carbon during vegetative growth. Under the hypothesis that grasses respond to environmental selective pressures, we analyzed the differences in certain leaf, culm, and regenerative traits of 283 native Uruguayan grasses growing in open (grassland) and shaded (forest) habitats. In order to differentiate the phylogenetic effects from the adaptive changes to current local conditions, we used phylogenetically controlled comparative analysis. We found that the divergence of grass species between grasslands and forests was accompanied by changes in leaf traits. Narrow and filiform blades (higher length/width ratio) were favored in species growing in grasslands, while wider and oval blades were favored in species growing in forests. The response of the leaf blades in forests was probably directed towards maximizing light interception, while in grasslands could be linked to the loss of water and heat. In contrast, we found that neither the culm nor the caryopsis length exhibited significant evolutionary changes associated with open or shaded habitats. Our results highlight the functional significance and adaptive value of the width and shape of the grass blades to the current environment.

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References

  • Ackerly DD (2003) Community assembly, niche conservatism, and adaptive evolution in changing environments. Int J Plant Sci 164:S165–S184

    Article  Google Scholar 

  • Ackerly DD, Reich PB (1999) Convergence and correlations among leaf size and function in seed plants: a comparative test using independent contrasts. Am J Bot 86:1272–1281

    Article  PubMed  CAS  Google Scholar 

  • Ackerly DD, Dudley SA, Sultan SE, Schmitt J, Coleman JS, Linder CR, Sandquist DR, Geber MA, Evans AS, Dawson TE, Lechowicz MJ (2000) The evolution of plant ecophysiological traits: recent advances and future directions. Bioscience 50:979–995

    Article  Google Scholar 

  • Ackerly DD, Knight CA, Weiss SB, Barton K, Starmer KP (2002) Leaf size, specific leaf area and microhabitat distribution of chaparral woody plants: contrasting patterns in species level and community level analyses. Oecologia 130:449–457

    Article  Google Scholar 

  • Aliscioni SS, Giussani LM, Zuloaga FO, Kellogg EA (2003) A molecular phylogeny of Panicum (Poaceae: Paniceae): tests of monophyly and phylogenetic placement within the Panicoideae. Am J Bot 90:796–821

    Article  PubMed  CAS  Google Scholar 

  • Baker HG (1972) Seed weight in relation to environmental conditions in California. Ecology 53:997–1010

    Article  Google Scholar 

  • Bess EC, Doust AN, Kellogg EA (2005) A naked grass in the “Bristle Clade”: a phylogenetic and developmental study of Panicum section Bulbosa (Paniceae: Poaceae). Int J Plant Sci 166:371–381

    Article  CAS  Google Scholar 

  • Brazeiro A, Achkar M, Canavero A, Fagúndez C, González E, Grela I, Lezama F, Maneyro R, Berthesagy L, Camargo A, Carreira S, Costa B, Núñez D, da Rosa I, Toranza C (2008) Prioridades geográficas para la conservación de la biodiversidad terrestre de Uruguay. PDT 32-26 Project

  • Brussa CA, Grela IA (2007) Flora arbórea del Uruguay. COFUSA, Uruguay

    Google Scholar 

  • Censo General Agropecuario (2000). DIEA. Ministerio de Ganadería, Agricultura y Pesca (MGAP), Uruguay. Available from http://www.mgap.gub.uy

  • Christin PA, Besnard G, Samaritani E, Duvall MR, Hodkinson TR, Savolainen V, Salamin N (2008) Oligocene CO2 decline promoted C4 photosynthesis in grasses. Curr Biol 18:37–43

    Article  PubMed  CAS  Google Scholar 

  • Cialdella AM, Giussani LM, Aagesen L, Zuloaga FO, Morrone O (2007) A phylogeny of Piptochaetium (Poaceae: Pooideae: Stipeae) and related genera based on a combined analysis including trnL-F, rpl16, and morphology. Syst Bot 32:545–559

    Article  Google Scholar 

  • Clayton WD, Harman KT, Williamson H (2002 onwards) World grass species: descriptions, identification, and information retrieval. Available from http://www.kew.org/data/grasses-db.html

  • Coughenour MB (1985) Graminoid responses to grazing by large herbivores: adaptations, exaptations, and interacting processes. Ann Mo Bot Gard 72:852–863

    Article  Google Scholar 

  • Cunningham SA, Summerhayes B, Westoby M (1999) Evolutionary divergences in leaf structure and chemistry, comparing rainfall and soil nutrient gradients. Ecology 69:569–588

    Google Scholar 

  • Donovan LA, Maherali H, Caruso CM, Huber H, de Kroon H (2011) The evolution of the worldwide leaf economics spectrum. Trends Ecol Evol 26:88–95

    Article  PubMed  Google Scholar 

  • Duvall MR, Noll JD, Minn AH (2001) Phylogenetics of Paniceae (Poaceae). Am J Bot 88:1988–1992

    Article  PubMed  CAS  Google Scholar 

  • Duvall MR, Davis JI, Clark LG, Noll JD, Goldman DH, Sánchez-Ken JG (2007) Phylogeny of the grasses (Poaceae) revisited. Aliso 23:237–247

    Google Scholar 

  • Edwards EJ, Smith SA (2010) Phylogenetic analyses reveal the shady history of C4 grasses. Proc Natl Acad Sci USA 107:2532–2537

    Article  PubMed  CAS  Google Scholar 

  • Edwards EJ, Still CJ (2008) Climate, phylogeny and the ecological distribution of C4 grasses. Ecol Lett 11:266–276

    Article  PubMed  Google Scholar 

  • Ehleringer JR, Monson RK (1993) Evolutionary and ecological aspects of photosynthetic pathway variation. Annu Rev Ecol Syst 24:411–439

    Article  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15

    Article  Google Scholar 

  • Foster SA (1986) On the adaptive value of large seeds for tropical moist forest trees: a review and synthesis. Bot Rev 52:260–299

    Article  Google Scholar 

  • Freckleton RP (2000) Phylogenetic tests of ecological and evolutionary hypotheses: checking for phylogenetic independence. Funct Ecol 14:129–134

    Article  Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using independent contrasts. Syst Biol 41:18–32

    Google Scholar 

  • Ge S, Li A, Lu BR, Zhang SZ, Hong DY (2002) A phylogeny of the rice tribe Oryzeae (Poaceae) based on matK sequence data. Am J Bot 89:1967–1972

    Article  PubMed  Google Scholar 

  • Gibson DJ (2009) Grasses and grassland ecology. Oxford University Press, New York

    Google Scholar 

  • Giussani LM, Cota-Sánchez JH, Zuloaga FO, Kellogg EA (2001) A molecular phylogeny of the grass subfamily Panicoideae (Poaceae) shows multiple origins of C4 photosynthesis. Am J Bot 88:1993–2012

    Article  PubMed  CAS  Google Scholar 

  • Givnish TJ (1979) On the adaptive significance of leaf form. In: Solbrig OT, Jain S, Johnson GB, Raven PH (eds) Topics in plant population biology. Macmillan, London, pp 375–407

    Google Scholar 

  • Givnish TJ (1982) On the adaptive significance of leaf height in forest herbs. Am Nat 120:353–381

    Article  Google Scholar 

  • Givnish TJ (1987) Comparative studies of leaf form: assessing the relative roles of selective pressures and phylogenetic constraints. New Phytol 106(Suppl.):131–160

    Google Scholar 

  • Givnish TJ (1988) Adaptation to sun and shade: a whole-plant perspective. Aust J Plant Physiol 15:63–92

    Article  Google Scholar 

  • Givnish TJ, Vermeij GJ (1976) Sizes and shapes of liane leaves. Am Nat 110:743–778

    Article  Google Scholar 

  • Grass Phylogeny Working Group (2001) Phylogeny and subfamilial classification of the grasses (Poaceae). Ann Mo Bot Gard 88:373–457

    Article  Google Scholar 

  • Grass Phylogeny Working Group II (2012) New grass phylogeny resolves deep evolutionary relationships and discovers C4 origins. New Phytol 193:304–312

    Article  Google Scholar 

  • Guo YL, Ge S (2005) Molecular phylogeny of Oryzeae (Poaceae) based on DNA sequences from chloroplast, mitochondrial, and nuclear genomes. Am J Bot 92:1548–1558

    Article  PubMed  CAS  Google Scholar 

  • Gurevitch J, Scheiner SM, Fox GA (2006) The ecology of plants, 2nd edn. Sinauer, Sunderland

  • Hallik L, Niinemets U, Wright IJ (2009) Are species shade and drought tolerance reflected in leaf-level structural and functional differentiation in Northern Hemisphere temperate woody flora? New Phytol 184:257–274

    Article  PubMed  CAS  Google Scholar 

  • Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electronica 4:1–9

    Google Scholar 

  • Harvey PH, Pagel MB (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

    Google Scholar 

  • Hewitt N (1998) Seed size and shade-tolerance: a comparative analysis of North American temperate trees. Oecologia 114:432–440

    Article  Google Scholar 

  • Hilu KW, Alice LA (2001) A phylogeny of Chloridoideae (Poaceae) based on matK sequences. Syst Bot 26:386–405

    Google Scholar 

  • Hodkinson DJ, Askew AP, Thompson K, Hodgson JG, Bakker JP, Bekker RM (1998) Ecological correlates of seed size in the British flora. Funct Ecol 12:762–766

    Article  Google Scholar 

  • Jacobs BF, Kingston DJ, Jacobs LL (1999) The origin of grass-dominated ecosystems. Ann Mo Bot Gard 86:590–643

    Article  Google Scholar 

  • Kellogg EA (1998) Relationships of cereal crops and other grasses. Proc Natl Acad Sci USA 95:2005–2010

    Article  PubMed  CAS  Google Scholar 

  • Kellogg EA (2001) Evolutionary history of the grasses. Plant Physiol 125:1198–1205

    Article  PubMed  CAS  Google Scholar 

  • Kellogg EA (2009) The evolutionary history of Ehrhartoideae, Oryzeae, and Oryza. Rice 2:1–14

    Article  Google Scholar 

  • Kellogg EA, Hiser KM, Doust AN (2004) Taxonomy, phylogeny, and inflorescence development of the genus Ixophorus (Panicoideae: Poaceae). Int J Plant Sci 165:1089–1105

    Article  Google Scholar 

  • Kelly CK (1996) Seed mass, habitat conditions and taxonomic relatedness: a reanalysis of Salisbury (1974). New Phytol 135:169–174

    Article  Google Scholar 

  • Kidson R, Westoby M (2000) Seed mass and seedling dimensions in relation to seedling establishment. Oecologia 125:11–17

    Article  Google Scholar 

  • Leishman MR, Westoby M (1994) The role of large seed size in shaded conditions: experimental evidence. Funct Ecol 8:205–214

    Article  Google Scholar 

  • Leishman MR, Wright IJ, Moles AT, Westoby M (2000) The evolutionary ecology of seed size. In: Fenner M (ed) Seeds: the ecology of regeneration in plant communities. CAB Int, Wallingford, pp 31–57

    Chapter  Google Scholar 

  • Mathews S, Spangler RE, Mason-Gamer RJ, Kellogg EA (2002) Phylogeny of Andropogoneae inferred from phytochrome B, GBSSI, and ndhF. Int J Plant Sci 163:441–450

    Article  Google Scholar 

  • Mazer SJ (1989) Ecological, taxonomic, and life history correlates of seed mass among Indiana Dune angiosperms. Ecol Monogr 59:153–175

    Article  Google Scholar 

  • Metcalfe DJ, Grubb PJ (1995) Seed mass and light requirement for regeneration in South-East Asian rain forest. Can J Bot 73:817–826

    Article  Google Scholar 

  • Milchunas DG, Sala OE, Lauenroth WK (1988) A generalized model of the effects of grazing by large herbivores on grassland community structure. Am Nat 132:87–106

    Article  Google Scholar 

  • Milla R, Reich PB (2007) The scaling of leaf area and mass: the cost of light interception increases with leaf size. Proc R Soc B 274:2109–2114

    Article  PubMed  Google Scholar 

  • Moles AT, Warton DI, Warman L, Swenson NG, Laffan SW, Zanne AE, Pitman A, Hemmings FA, Leishman MR (2009) Global patterns in plant height. J Ecol 97:923–932

    Article  Google Scholar 

  • Osborne CP, Freckleton RP (2009) Ecological selection pressures for C4 photosynthesis in the grasses. Proc R Soc B 276:1753–1760

    Article  PubMed  Google Scholar 

  • Oyarzabal M, Paruelo JM, del Pino F, Oesterheld M, Lauenroth W (2008) Trait differences between grass species along a climatic gradient in South and North America. J Veg Sci 19:183–192

    Article  Google Scholar 

  • Pagani M, Freeman KH, Arthur MA (1999) Late Miocene atmospheric CO2 concentrations and the expansion of C4 grasses. Science 285:876–879

    Article  PubMed  CAS  Google Scholar 

  • Pagel M (1992) A method for analysis of comparative data. J Theor Biol 156:431–442

    Article  Google Scholar 

  • Parkhurst DF, Loucks OL (1972) Optimal leaf size in relation to environment. J Ecol 60:505–537

    Article  Google Scholar 

  • Petersen G, Seberg O (2003) Phylogenetic analyses of the diploid species of Hordeum (Poaceae) and a revised classification of the genus. Syst Bot 28:293–306

    Google Scholar 

  • Poorter L (1999) Growth responses of 15 rain-forest tree species to a light gradient: the relative importance of morphological and physiological traits. Funct Ecol 13:396–410

    Article  Google Scholar 

  • Poorter L, Wright SJ, Paz H, Ackerly DD, Condit R, Ibarra-Manríquez G, Harms KE, Lincona JC, Martínez-Ramos M, Mazer SJ, Muller-Landau HC, Peña-Claros M, Webb CO, Wright IJ (2008) Are functional traits good predictors of demographic rates? Evidence from five Neotropical forests. Ecology 89:1908–1920

    Article  PubMed  CAS  Google Scholar 

  • Purvis A, Rambaut A (1995) Comparative analysis by independent contrasts (CAIC): an Apple Macintosh application for analysing comparative data. Comput Appl Biosci 11:247–251

    PubMed  CAS  Google Scholar 

  • Quintanar A, Castroviejo S, Catalán P (2007) Phylogeny of the tribe Aveneae (Pooideae, Poaceae) inferred from plastid trnT-F and nuclear ITS sequences. Am J Bot 94:1554–1569

    Article  PubMed  CAS  Google Scholar 

  • Redmann RE (1985) Adaptation of grasses to water stress-leaf rolling and stomata distribution. Ann Mo Bot Gard 72:833–842

    Article  Google Scholar 

  • Reich PB, Wright IJ, Cavender-Bares J, Craine JM, Oleksyn J, Westoby M, Walters MB (2003) The evolution of plant functional variation: traits, spectra and strategies. Int J Plant Sci 164:s143–s164

    Article  Google Scholar 

  • Ripley BS, Frole K, Gilbert M (2010) Differences in drought sensitivities and photosynthetic limitations between co-occurring C3 and C4 (NADP-ME) Panicoid grasses. Ann Bot 105:493–503

    Article  PubMed  CAS  Google Scholar 

  • Rosengurtt B, Arrillaga BR, Izaguirre P (1970) Gramíneas uruguayas. Universidad de la República, Montevideo

    Google Scholar 

  • Sage RF (2004) The evolution of C4 photosynthesis. New Phytol 161(2):341–370

    Article  CAS  Google Scholar 

  • Sage RF, Wedin DA, Li M (1999) The biogeography of C4 photosynthesis: patterns and controlling factors. In: Sage RF, Monson RK (eds) C4 plant biology. Academic Press, San Diego, pp 313–373

    Chapter  Google Scholar 

  • Salisbury EJ (1942) The reproductive capacity of plants. G Bell and Sons, London

    Google Scholar 

  • Salisbury EJ (1974) Seed size and mass in relation to environment. Proc R Soc Lond B 186:83–88

    Article  Google Scholar 

  • Sánchez-Ken JG, Clark LG, Kellogg EA, Kay EE (2007) Reinstatement and emendation of subfamily Micrairoideae (Poaceae). Syst Bot 32:71–80

    Article  Google Scholar 

  • Saverimuttu T, Westoby M (1996) Seedling longevity under deep shade in relation to seed size. J Ecol 84:681–689

    Article  Google Scholar 

  • Silvertown JW, Dodd M (1997) Comparing plants and connecting traits. In: Silvertown JW, Franco M, Harper JL (eds) Plant life histories: ecology, phylogeny and evolution. Cambridge University Press, New York, pp 3–16

    Google Scholar 

  • Soreng RJ, Davis JI, Voionmaa MA (2007) A phylogenetic analysis of Poaceae tribe Poeae sensu lato based on morphological characters and sequence data from three plastid-encoded genes: evidence for reticulation, and a new classification for the tribe. Kew Bull 62:425–454

    Google Scholar 

  • Soriano A (1992) Río de la Plata grasslands. In: Coupland RT (ed) Natural grasslands: introduction and western hemisphere. Ecosystems of the world, vol 8A. Elsevier, Amsterdam, pp 367–407

    Google Scholar 

  • Strömberg CAE (2011) Evolution of grasses and grassland ecosystems. Annu Rev Earth Planet Sci 39:517–544

    Article  Google Scholar 

  • Taylor SH, Ripley BS, Woodward FI, Osborne CP (2011) Drought limitation of photosynthesis differs between C3 and C4 grass species in a comparative experiment. Plant, Cell Environ 34:65–75

    Article  CAS  Google Scholar 

  • Tropicos.org. Missouri Botanical Garden. Available from http://www.tropicos.org

  • Tullberg BS, Hunter AF (1996) Evolution of larval gregariousness in relation to repellent defences and warning coloration in tree-feeding Macrolepidoptera: a phylogenetic analysis based on independent contrasts. Biol J Linn Soc 57:253–276

    Article  Google Scholar 

  • Verboom G, Linder AHP, Stock WD (2004) Testing the adaptive nature of radiation: growth form and life history divergence in the African grass genus Ehrharta (Poaceae: Ehrhartoideae). Am J Bot 91:1364–1370

    Article  PubMed  Google Scholar 

  • Vicentini A, Barber JC, Aliscioni SS, Giussani M, Kellogg EA (2008) The age of the grasses and clusters of origins of C4 photosynthesis. Glob Change Biol 14:2963–2977

    Article  Google Scholar 

  • Villar R, Veneklaas EJ, Jordano P, Lambers H (1998) Relative growth rate and biomass allocation in 20 Aegilops (Poaceae) species. New Phytol 140:425–437

    Article  Google Scholar 

  • Vogel S (1968) “Sun leaves” and “shade leaves”: differences in convective heat dissipation. Ecology 49:1203–1204

    Article  Google Scholar 

  • Walters MB, Reich PB (2000) Seed size, nitrogen supply and growth rate affect tree seedling survival in deep shade. Ecology 81:1887–1901

    Article  Google Scholar 

  • Westoby M (1998) A leaf-height-seed (LHS) plant ecology strategy scheme. Plant Soil 199:213–227

    Article  CAS  Google Scholar 

  • Westoby M, Leishman M, Lord J, Poorter H, Schoen DJ (1996) Comparative ecology of seed size and dispersal. Philos Trans R Soc Lond B 351:1309–1318

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wright IJ, Leishman MR, Read C, Westoby M (2006) Gradients of light availability and leaf traits with leaf age and canopy position in 28 Australian shrubs and trees. Funct Plant Biol 33:407–419

    Article  Google Scholar 

  • Zar J (1996) Biostatistical analysis, 3rd edn. Prentice-Hall, New Jersey

    Google Scholar 

  • Zhang W (2000) Phylogeny of the grass family (Poaceae) from rpl16 intron sequence data. Mol Phylogenet Evol 15(1):135–146

    Article  PubMed  CAS  Google Scholar 

  • Zuloaga FO, Nicora EG, Rúgolo De Agrasar ZE, Morrone O, Pensiero J, Cialdella AM (1994) Catálogo de la familia Poaceae en la República Argentina. Monogr Syst Bot Mo Bot Gard 47:1–178

    Google Scholar 

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Acknowledgments

We thank Alejandro Brazeiro for providing access to the database PDT 32-26 Project, and Felipe Lezama for clarifying several questions related to grass taxonomy. F. Maruri, W. Ferrer, C. and F. Harte and M. Root-Bernstein patiently revised the style of the paper. Dr. H. Maherali and two anonymous reviewers made very useful commentaries to earlier drafts of the manuscript. This study was partially funded by the Comisión Sectorial de Investigación Científica (CSIC) of the Universidad de la República (Uruguay).

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  1. Instituto de Ecología y Ciencias Ambientales, Facultad de Ciencias, Iguá 4225, Montevideo, Uruguay

    Valerie Cayssials & Claudia Rodríguez

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  1. Valerie Cayssials
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Correspondence to Claudia Rodríguez.

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Cayssials, V., Rodríguez, C. Functional traits of grasses growing in open and shaded habitats. Evol Ecol 27, 393–407 (2013). https://doi.org/10.1007/s10682-012-9601-3

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