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Leaf thickness controls variation in leaf mass per area (LMA) among grazing-adapted grasses in Serengeti

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Abstract

Leaf mass per area (LMA) is a primary plant functional trait that represents the cost of constructing a leaf. Ultimately, plants modify LMA by altering leaf thickness (LT), leaf dry matter content (LDMC), or both. While LMA can be modified through both of these constituents, studies of LMA have found that there is variation in whether LT or LDMC changes are responsible for LMA—and the relationships change depending on the species or functional groups being compared. In this study, we used a phylogenetic framework to determine that evolutionary shifts in LMA are driven by LT, and not LDMC, among 45 Serengeti grass species. We considered two alternative hypotheses that could result in evolutionary correlation of LMA on LT but not LDMC: either (1) LT is more labile than LDMC—and is therefore a less costly means to change LMA or (2) LDMC is tightly coupled to a different dimension of leaf variation (e.g., leaf hydraulics), leaving LT as the source of variation in LMA. LT was not more labile than LDMC, leading us to conclude that the evolution of LMA has been shaped by LT because LDMC is responding to other demands on leaf physiology. We speculate that leaf hydraulics provide this constraint on LDMC. The decoupling of LDMC from LT may allow plants to better optimize resource allocation in ecosystems where gradients in light competition, herbivory, and aridity place competing demands on leaf economics.

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References

  • Anderson TM, Dempewolf J, Metzger KL, Reed DN, Serneels S (2008) Generation and maintenance of heterogeneity in the Serengeti ecosystem. In: Serengeti III: human impacts on ecosystem dynamics, pp 135–182

  • Anderson TM, Shaw J, Olff H (2011) Ecology’s cruel dilemma, phylogenetic trait evolution and the assembly of Serengeti plant communities. J Ecol 99:797–806

    Article  Google Scholar 

  • Anderson TM, Kumordzi BB, Fokkema W et al (2013) Distinct physiological responses underlie defoliation tolerance in African lawn and bunch grasses. Int J Plant Sci 174:769–778. doi:10.1086/670237

    Article  Google Scholar 

  • Belsky AJ (1984) Small-scale pattern in grassland communities in the Serengeti National Park, Tanzania. Plant Ecol 55:141–151

    Article  Google Scholar 

  • Belsky AJ (1988) Regional influences on small-scale vegetational heterogeneity within grasslands in the Serengeti National Park, Tanzania. Plant Ecol 74:3–10

    Article  Google Scholar 

  • Blomberg SP, Garland JR, Ives AR (2003) Testing for phylogenetic signal in comparative data: behavioral traits are more labile. Evolution 57:717–745

    Article  PubMed  Google Scholar 

  • Edwards EJ, Chatelet DS, Sack L, Donoghue MJ (2014) Leaf life span and the leaf economic spectrum in the context of whole plant architecture. J Ecol 102:328–336. doi:10.1111/1365-2745.12209

    Article  Google Scholar 

  • Evans JR, Poorter H (2001) Photosynthetic acclimation of plants to growth irradiance: the relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain. Plant Cell Environ 24:755–767. doi:10.1046/j.1365-3040.2001.00724.x

    Article  CAS  Google Scholar 

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15. doi:10.1086/284325

    Article  Google Scholar 

  • Garland T, Midford PE, Ives AR (1999) An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral values. Am Zool 39:374–388

    Article  Google Scholar 

  • Garnier E, Laurent G (1994) Leaf anatomy, specific mass and water content in congeneric annual and perennial grass species. New Phytol 128:725–736

    Article  Google Scholar 

  • Garnier E, Shipley B, Roumet C, Laurent G (2001) A standardized protocol for the determination of specific leaf area and leaf dry matter content. Funct Ecol 15:688–695. doi:10.1046/j.0269-8463.2001.00563.x

    Article  Google Scholar 

  • Grime JP (1977) Evidence for the existence of three primary strategies in plants and its relevance to ecological and evolutionary theory. Am Nat 111:1169–1194. doi:10.1086/283244

    Article  Google Scholar 

  • Hartvigsen AG, McNaughton SJ (1995) Tradeoff between height and relative growth rate in a dominant grass from the Serengeti ecosystem. Ecology 102:273–276

    Google Scholar 

  • Holdo RM, Nippert JB (2015) Transpiration dynamics support resource partitioning in African savanna trees and grasses. Ecology 96:1466–1472. doi:10.1890/14-1986.1

    Article  Google Scholar 

  • Holdo RM, Holt RD, Fryxell JM (2009) Opposing rainfall and plant nutritional gradients best explain the wildebeest migration in the Serengeti. Am Nat 173:431–445

    Article  PubMed  Google Scholar 

  • Kembel SW, Cowan PD, Helmus MR et al (2010) Picante: R tools for integrating phylogenies and ecology. Bioinformatics 26:1463–1464

    Article  CAS  PubMed  Google Scholar 

  • Kim S (2012) ppcor: Partial and semi-partial (part) correlation. http://cran.r-project.org/package=ppcor

  • Li L, McCormack ML, Ma C et al (2015) Leaf economics and hydraulic traits are decoupled in five species-rich tropical–subtropical forests. Ecol Lett 18:899–906. doi:10.1111/ele.12466

    Article  CAS  PubMed  Google Scholar 

  • McNaughton SJ (1983) Serengeti grassland ecology: the role of composite environmental factors and contingency in community organization. Ecol Monogr 53:291–320

    Article  Google Scholar 

  • Niinemets Ü (1999) Research review. Components of leaf dry mass per area—thickness and density—alter leaf photosynthetic capacity in reverse directions in woody plants. New Phytol 144:35–47

    Article  Google Scholar 

  • Niinemets Ü (2001) Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82:453–469

    Article  Google Scholar 

  • Osborne CP, Salomaa A, Kluyver TA et al (2014) A global database of C4 photosynthesis in grasses. New Phytol 204:441–446. doi:10.1111/nph.12942

    Article  CAS  PubMed  Google Scholar 

  • Pérez-Harguindeguy N, Díaz S, Garnier E et al (2013) New handbook for standardised measurement of plant functional traits worldwide. Aust J Bot 61:167–234. doi:10.1071/BT12225

    Article  Google Scholar 

  • Poorter H, Niinemets Ü, Poorter L et al (2009) Causes and consequences of variation in leaf mass per area (LMA): a meta-analysis. New Phytol 182:565–588. doi:10.1111/j.1469-8137.2009.02830.x

    Article  PubMed  Google Scholar 

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Development Core Team, Vienna

    Google Scholar 

  • Reich PB (2014) The world-wide “fast–slow” plant economics spectrum: a traits manifesto. J Ecol 102:275–301. doi:10.1111/1365-2745.12211

    Article  Google Scholar 

  • Reich PB, Ellsworth DS, Walters MB et al (1999) Generality of leaf trait relationships: a test across six biomes. Ecology 80:1955–1969

    Article  Google Scholar 

  • Renton M, Poorter H (2011) Using log–log scaling slope analysis for determining the contributions to variability in biological variables such as leaf mass per area: why it works, when it works and how it can be extended. New Phytol 190:5–8

    Article  PubMed  Google Scholar 

  • Sack L, Scoffoni C, John GP et al (2014) Leaf mass per area is independent of vein length per area: avoiding pitfalls when modelling phenotypic integration (reply to Blonder et al. 2014). J Exp Bot 65:5115–5123. doi:10.1093/jxb/eru305

    Article  PubMed  PubMed Central  Google Scholar 

  • Sanchez A, Smith W (2012) Plant functional traits: perspectives from a quantitative literature review. Curr Trends Ecol 3:25–51

    Google Scholar 

  • Shipley B, Lechowicz MJ, Wright I, Reich PB (2006) Fundamental trade-offs generating the worldwide leaf economics spectrum. Ecology 87:535–541. doi:10.1890/05-1051

    Article  PubMed  Google Scholar 

  • Smith WK, Vogelmann TC, DeLucia EH et al (1997) Leaf form and photosynthesis. Biosciences 47:785–793

    Article  Google Scholar 

  • Smith WK, Vogelmann TC, Critchley C (eds) (2004) Photosynthetic adaptation: chloroplast to landscape. Springer, New York

    Google Scholar 

  • Vaieretti MV, Diaz S, Vile D, Garnier E (2007) Two measurement methods of leaf dry matter content produce similar results in a broad range of species. Ann Bot 99:955–958. doi:10.1093/aob/mcm022

    Article  PubMed  PubMed Central  Google Scholar 

  • Vile D, Garnier E, Shipley B et al (2005) Specific leaf area and dry matter content estimate thickness in laminar leaves. Ann Bot 96:1129–1136. doi:10.1093/aob/mci264

    Article  PubMed  PubMed Central  Google Scholar 

  • Villar R, Ruiz-Robleto J, Ubera JL, Poorter H (2013) Exploring variation in leaf mass per area (LMA) from leaf to cell: an anatomical analysis of 26 woody species. Am J Bot 100:1969–1980. doi:10.3732/ajb.1200562

    Article  PubMed  Google Scholar 

  • Violle C, Enquist BJ, McGill BJ et al (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252. doi:10.1016/j.tree.2011.11.014

    Article  PubMed  Google Scholar 

  • Warton DI, Duursma RA, Falster DS, Taskinen S (2012) smatr 3—an R package for estimation and inference about allometric lines. Methods Ecol Evol 3:257–259. doi:10.1111/j.2041-210X.2011.00153.x

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wilson PJ, Thompson KEN, Hodgson JG (1999) Specific leaf area and leaf dry matter content as alternative predictors of plant strategies. New Phytol 143:155–162

    Article  Google Scholar 

  • Witkowski ETF, Lamont BB (1991) Leaf specific mass confounds leaf density and thickness. Oecologia 88:486–493

    Article  Google Scholar 

  • Wright IJ, Reich PB, Westoby M et al (2004) The worldwide leaf economics spectrum. Nature 428:821–827

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The authors would like to thank Jeremia Sarakikya for help with data collection. DMG was supported by the National Science Foundation Graduate Research Fellowship under Grant No. 0907738, Richter Fellowship, Botanical Society of America Graduate Research Award, and Vecellio Award. TMA was supported by Grant DEB-1145861 from the National Science Foundation.

Author contribution statement

DMG, TMA, and KMQ conceived, designed, and performed the experiments. DMG analyzed the data and wrote the first draft of the manuscript; other authors provided editorial advice.

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Correspondence to Daniel M. Griffith.

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Communicated by Miquel Gonzalez-Meler.

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Griffith, D.M., Quigley, K.M. & Anderson, T.M. Leaf thickness controls variation in leaf mass per area (LMA) among grazing-adapted grasses in Serengeti. Oecologia 181, 1035–1040 (2016). https://doi.org/10.1007/s00442-016-3632-3

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