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Fossil leaf economics quantified: calibration, Eocene case study, and implications

  • Dana L. Royer (a1), Lawren Sack (a2), Peter Wilf (a3), Bárbara Cariglino (a3), Christopher H. Lusk (a4), Ian J. Wright (a4), Mark Westoby (a4), Gregory J. Jordan (a5), Ülo Niinemets (a6), Phyllis D. Coley (a7), Asher D. Cutter (a8), Conrad C. Labandeira (a8), Matthew B. Palmer (a8), Kirk R. Johnson (a9), Angela T. Moles (a4) and Fernando Valladares (a10)...

Abstract

Leaf mass per area (MA) is a central ecological trait that is intercorrelated with leaf life span, photosynthetic rate, nutrient concentration, and palatability to herbivores. These coordinated variables form a globally convergent leaf economics spectrum, which represents a general continuum running from rapid resource acquisition to maximized resource retention. Leaf economics are little studied in ancient ecosystems because they cannot be directly measured from leaf fossils. Here we use a large extant data set (65 sites; 667 species-site pairs) to develop a new, easily measured scaling relationship between petiole width and leaf mass, normalized for leaf area; this enables MA estimation for fossil leaves from petiole width and leaf area, two variables that are commonly measurable in leaf compression floras. The calibration data are restricted to woody angiosperms exclusive of monocots, but a preliminary data set (25 species) suggests that broad-leaved gymnosperms exhibit a similar scaling. Application to two well-studied, classic Eocene floras demonstrates that MA can be quantified in fossil assemblages. First, our results are consistent with predictions from paleobotanical and paleoclimatic studies of these floras. We found exclusively low-MA species from Republic (Washington, U.S.A., 49 Ma), a humid, warm-temperate flora with a strong deciduous component among the angiosperms, and a wide MA range in a seasonally dry, warm-temperate flora from the Green River Formation at Bonanza (Utah, U.S.A., 47 Ma), presumed to comprise a mix of short and long leaf life spans. Second, reconstructed MA in the fossil species is negatively correlated with levels of insect herbivory, whether measured as the proportion of leaves with insect damage, the proportion of leaf area removed by herbivores, or the diversity of insect-damage morphotypes. These correlations are consistent with herbivory observations in extant floras and they reflect fundamental trade-offs in plant-herbivore associations. Our results indicate that several key aspects of plant and plant-animal ecology can now be quantified in the fossil record and demonstrate that herbivory has helped shape the evolution of leaf structure for millions of years.

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Ackerly, D. D., and Reich, P. B. 1999. Convergence and correlations among leaf size and function in seed plants: a comparative test using independent contrasts. American Journal of Botany 86: 12721281.
Beck, A. L., and Labandeira, C. C. 1998. Early Permian insect folivory on a gigantopterid-dominated riparian flora from north-central Texas. Palaeogeography, Palaeoclimatology, Palaeoecology 142: 139173.
Brentnall, S. J., Beerling, D. J., Osborne, C. P., Harland, M., Francis, J. E., Valdes, P. J., and Wittig, V. E. 2005. Climatic and ecological determinants of leaf lifespan in polar forests of the high CO2 Cretaceous ‘greenhouse’ world. Global Change Biology 11: 21772195.
Chaloner, W. G., and Creber, G. T. 1990. Do fossil plants give a climatic signal? Journal of the Geological Society, London 147: 343350.
Chapin, F. S. 2003. Effects of plant traits on ecosystem and regional processes: a conceptual framework for predicting the consequences of global change. Annals of Botany 91: 455463.
Coley, P. D. 1983. Herbivory and defensive characteristics of tree species in a lowland tropical forest. Ecological Monographs 53: 209233.
Cornelissen, J. H. C., Lavorel, S., Garnier, E., Díaz, S., Buchmann, N., Gurvich, D. E., Reich, P. B., ter Steege, H., Morgan, H. D., van der Heijden, M. G. A., Pausas, J. G., and Poorter, H. 2003. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Australian Journal of Botany 51: 335380.
Díaz, S., Hodgson, J. G., Thompson, K., Cabido, M., Cornelissen, J. H. C., Jalili, A., Montserrat-Martí, G., Grime, J. P., Zarrinkamar, F., Asri, Y., Band, S. R., Basconcelo, S., Castro-Díez, P., Funes, G., Hamzehee, B., Khoshnevi, M., Pérez-Harguindeguy, N., Pérez-Rontomé, M. C., Shirvany, F. A., Vendramini, F., Yazdani, S., Abbas-Azimi, R., Bogaard, A., Boustani, S., Charles, M., Dehghan, M., de Torres-Espuny, L., Falczuk, V., Guerrero-Campo, J., Hynd, A., Jones, G., Kowsary, E., Kazemi-Saeed, F., Maestro-Martinez, M., Romo-Díez, A., Shaw, S., Siavash, B., Villar-Salvador, P., and Zak, M. R. 2004. The plant traits that drive ecosystems: evidence from three continents. Journal of Vegetation Science 15: 295304.
Falcon-Lang, H. J. 2000a. A method to distinguish between woods produced by evergreen and deciduous coniferopsids on the basis of growth ring anatomy: a new palaeoecological tool. Palaeontology 43: 785793.
Falcon-Lang, H. J. 2000b. The relationship between leaf longevity and growth ring markedness in modern conifer woods and its implications for palaeoclimatic studies. Palaeogeography, Palaeoclimatology, Palaeoecology 160: 317328.
Falster, D. S., Warton, D. I., and Wright, I. J. 2003. (S)MATR: standardised major axis tests and routines. Version 1.0. http://www.bio.mq.edu.au/ecology/SMATR.
Greenwood, D. R., Archibald, S. B., Mathewes, R. W., and Moss, P. T. 2005. Fossil biotas from the Okanagan Highlands, southern British Columbia and northeastern Washington State: climates and ecosystems across an Eocene landscape. Canadian Journal of Earth Sciences 42: 167185.
Grime, J. P. 1974. Vegetation classification by reference to strategies. Nature 250: 2631.
Grubb, P. J. 1998. A reassessment of the strategies of plants which cope with shortages of resources. Perspectives in Plant Ecology, Evolution and Systematics 1: 331.
Huff, P. M., Wilf, P., and Azumah, E. J. 2003. Digital future for paleoclimate estimation from fossil leaves? Preliminary results. Palaios 18: 266274.
Kazakou, E., Vile, D., Shipley, B., Gallet, C., and Garnier, E. 2006. Co-variations in litter decomposition, leaf traits and plant growth in species from a Mediterranean old-field succession. Functional Ecology 20: 2130.
Kobe, R. K., Lepczyk, C. A., and Iyer, M. 2005. Resorption efficiency decreases with increasing green leaf nutrients in a global data set. Ecology 86: 27802792.
Kowalski, E. A., and Dilcher, D. L. 2003. Warmer paleotemperatures for terrestrial ecosystems. Proceedings of the National Academy of Sciences USA 100: 167170.
Labandeira, C. C. 1998. Early history of arthropod and vascular plant associations. Annual Review of Earth and Planetary Sciences 26: 329377.
Labandeira, C. C. 2002. Paleobiology of middle Eocene plant-insect associations from the Pacific Northwest: a preliminary report. Rocky Mountain Geology 37: 3159.
MacGinitie, H. D. 1969. The Eocene Green River flora of northwestern Colorado and northeastern Utah. University of California Publications in Geological Sciences 83: 1202.
McMahon, T. A., and Bonner, J. T. 1983. On size and life. Scientific American Library, New York.
Moles, A. T., and Westoby, M. 2000. Do small leaves expand faster than large leaves, and do shorter expansion times reduce herbivore damage? Oikos 90: 517524.
Nardini, A., Gortan, E., and Salleo, S. 2005. Hydraulic efficiency of the leaf venation system in sun- and shade-adapted species. Functional Plant Biology 32: 953961.
New, M., Lister, D., Hulme, M., and Makin, I. 2002. A high-resolution data set of surface climate over global land areas. Climate Research 21: 125 (data available at http://www.cru.uea.ac.uk/cru/data/tmc.htm).
Niinemets, Ü. 2001. Global-scale climatic controls of leaf dry mass per area, density, and thickness in trees and shrubs. Ecology 82: 453469.
Niinemets, Ü., Valladares, F., and Ceulemans, R. 2003. Leaf-level phenotypic variability and plasticity of invasive Rhododendron ponticum and non-invasive Ilex aquifolium co-occurring at two contrasting European sites. Plant, Cell and Environment 26: 941956.
Niinemets, Ü., Portsmuth, A., Tena, D., Tobias, M., Matesanz, S., and Valladares, F. 2007. Do we underestimate the importance of leaf size in plant economics? Disproportionate scaling of support costs within the spectrum of leaf physiognomy. Annals of Botany 100: 283303.
Niklas, K. J. 1978. Morphometric relationships and rates of evolution among Paleozoic vascular plants. Evolutionary Biology 11: 509543.
Niklas, K. J. 1991a. The elastic-moduli and mechanics of Populus tremuloides (Salicaceae) petioles in bending and torsion. American Journal of Botany 78: 989996.
Niklas, K. J. 1991b. Flexural stiffness allometries of angiosperm and fern petioles and rachises: evidence for biomechanical convergence. Evolution 45: 734750.
Niklas, K. J. 1994. Plant allometry: the scaling of form and function. University of Chicago Press, Chicago.
Niklas, K. J. 1996. Differences between Acer saccharum leaves from open and wind-protected sites. Annals of Botany 78: 6166.
Niklas, K. J. 1998. The influence of gravity and wind on land plant evolution. Review of Palaeobotany and Palynology 102: 114.
Niklas, K. J. 1999. A mechanical perspective on foliage leaf form and function. New Phytologist 143: 1931.
Parton, W., Silver, W. L., Burke, I. C., Grassens, L., Harmon, M. E., Currie, W. S., King, J. Y., Adair, E. C., Brandt, L. A., Hart, S. C., and Fasth, B. 2007. Global-scale similarities in nitrogen release patterns during long-term decomposition. Science 315: 361364.
Peters, R. H. 1983. The ecological implications of body size. Cambridge University Press, Cambridge.
Poorter, L., and Bongers, F. 2006. Leaf traits are good predictors of plant performance across 53 rain forest species. Ecology 87: 17331743.
Poorter, L., van de Plassche, M., Willems, S., and Boot, R. G. A. 2004. Leaf traits and herbivory rates of tropical tree species differing in successional status. Plant Biology 6: 746754.
Radtke, M. G., Pigg, K. B., and Wehr, W. C. 2005. Fossil Corylopsis and Fothergilla leaves (Hamamelidaceae) from the lower Eocene flora of Republic, Washington, USA, and their evolutionary and biogeographic significance. International Journal of Plant Sciences 166: 347356.
Reich, P. B., Walters, M. B., and Ellsworth, D. S. 1997. From tropics to tundra: global convergence in plant function. Proceedings of the National Academy of Sciences USA 94: 1373013734.
Rex, G. M. 1986. Further experimental investigations on the formation of plant compression fossils. Palaios 19: 143159.
Rex, G. M., and Chaloner, W. G. 1983. The experimental formation of plant compression fossils. Palaeontology 26: 231252.
Royer, D. L., Osborne, C. P., and Beerling, D. J. 2002. High CO2 increases the freezing sensitivity of plants: implications for paleoclimatic reconstructions from fossil floras. Geology 30: 963966.
Royer, D. L., Wilf, P., Janesko, D. A., Kowalski, E. A., and Dilcher, D. L. 2005. Correlating climate and plant ecology with leaf size and shape: potential proxies for the fossil record. American Journal of Botany 92: 11411151.
Sack, L., and Frole, K. 2006. Leaf structural diversity is related to hydraulic capacity in tropical rainforest trees. Ecology 87: 483491.
Sack, L., Melcher, P. J., Zwieniecki, M. A., and Holbrook, N. M. 2002. The hydraulic conductance of the angiosperm leaf lamina: a comparison of three measurement methods. Journal of Experimental Botany 53: 21772184.
Sack, L., Cowan, P. D., Jaikumar, N., and Holbrook, N. M. 2003. The ‘hydrology’ of leaves: co-ordination of structure and function in temperate woody species. Plant, Cell and Environment 26: 13431356.
Sack, L., Tyree, M. T., and Holbrook, N. M. 2005. Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytologist 167: 403413.
Salisbury, E. J. 1913. The determining factors in petiolar structure. New Phytologist 12: 281289.
Schmidt-Nielsen, K. 1984. Scaling. Cambridge University Press, Cambridge.
Shipley, B., Vile, D., and Garnier, É. 2006. From plant traits to plant communities: a statistical mechanistic approach to biodiversity. Science 314: 812814.
Small, E. 1972. Photosynthetic rates in relation to nitrogen recycling as an adaptation to nutrient deficiency in peat bog plants. Canadian Journal of Botany 50: 22272233.
Smith, M. E., Carroll, A. R., and Singer, B. S. 2007. Synoptic reconstruction of a major ancient lake system: Eocene Green River Formation, Western United States. Geological Society of America Bulletin (in press).
Sokal, R. R., and Rohlf, F. J. 1995. Biometry, 3d ed. W.H. Freeman, New York.
Spicer, R. A. 1981. The sorting and deposition of allochthonous plant material in a modern environment at Silwood Lake, Silwood Park, Berkshire, England. U.S. Geological Survey Professional Paper 1143: 177.
Spicer, R. A., and Parrish, J. T. 1986. Paleobotanical evidence for cool north polar climates in middle Cretaceous (Albian-Cenomanian) time. Geology 14: 703706.
Thomas, S. C., and Winner, W. E. 2002. Photosynthetic differences between saplings and adult trees: an integration of field results by meta-analysis. Tree Physiology 22: 117127.
Villar, R., and Merino, J. 2001. Comparison of leaf construction costs in woody species with differing leaf life-spans in contrasting ecosystems. New Phytologist 151: 213226.
Walton, J. 1936. On the factors which influence the external form of fossil plants; with descriptions of the foliage of some species of the Palaeozoic equisetalean genus Annularia Sternberg. Philosophical Transactions of the Royal Society of London B 226: 219237.
Warton, D. I., Wright, I. J., Falster, D. S., and Westoby, M. 2006. Bivariate line-fitting methods for allometry. Biological Reviews 81: 259291.
Westoby, M., Falster, D. S., Moles, A. T., Vesk, P. A., and Wright, I. J. 2002. Plant ecological strategies: some leading dimensions of variation between species. Annual Review of Ecology and Systematics 33: 125159.
Whittaker, R. 1975. Communities and ecosystems. Macmillan, New York.
Wilf, P., and Labandeira, C. C. 1999. Response of plant-insect associations to Paleocene-Eocene warming. Science 284: 21532156.
Wilf, P., Wing, S. L., Greenwood, D. R., and Greenwood, C. L. 1998. Using fossil leaves as paleoprecipitation indicators: an Eocene example. Geology 26: 203206.
Wilf, P., Labandeira, C. C., Johnson, K. R., Coley, P. D., and Cutter, A. D. 2001. Insect herbivory, plant defense, and early Cenozoic climate change. Proceedings of the National Academy of Sciences USA 98: 62216226.
Wilf, P., Labandeira, C. C., Johnson, K. R., and Cúneo, N. R. 2005. Richness of plant-insect associations in Eocene Patagonia: a legacy for South American biodiversity. Proceedings of the National Academy of Sciences USA 102: 89448948.
Wing, S. L., and Greenwood, D. R. 1993. Fossils and fossil climate: the case for equable continental interiors in the Eocene. Philosophical Transactions of the Royal Society London B 341: 243252.
Wolfe, J. A. 1987. Late Cretaceous-Cenozoic history of deciduousness and the terminal Cretaceous event. Paleobiology 13: 215226.
Wolfe, J. A., and Upchurch, G. R. 1987. Leaf assemblages across the Cretaceous-Tertiary boundary in the Raton Basin, New Mexico and Colorado. Proceedings of the National Academy of Sciences USA 84: 50965100.
Wolfe, J. A., and Wehr, W. C. 1987. Middle Eocene dicotyledonous plants from Republic, northeastern Washington. U.S. Geological Survey Bulletin 1597: 125.
Wright, I. J., and Westoby, M. 2002. Leaves at low versus high rainfall: coordination of structure, lifespan and physiology. New Phytologist 155: 403416.
Wright, I. J., Reich, P. B., and Westoby, M. 2001. Strategy-shifts in leaf physiology, structure and nutrient content between species of high and low rainfall, and high and low nutrient habitats. Functional Ecology 15: 423434.
Wright, I. J., Reich, P. B., Westoby, M., Ackerly, D. D., Baruch, Z., Bongers, F., Cavender-Bares, J., Chapin, T., Cornelissen, J. H. C., Diemer, M., Flexas, J., Garnier, E., Groom, P. K., Gulias, J., Hikosaka, K., Lamont, B. B., Lee, T., Lee, W., Lusk, C., Midgley, J. J., Navas, M.-L., Niinemets, Ü., Oleksyn, J., Osada, N., Poorter, H., Poot, P., Prior, L., Pyankov, V. I., Roumet, C., Thomas, S. C., Tjoelker, M. G., Veneklaas, E. J., and Villar, R. 2004. The worldwide leaf economics spectrum. Nature 428: 821827.
Wright, I. J., Reich, P. B., Cornelissen, J. H. C., Falster, D. S., Groom, P. K., Hikosaka, K., Lee, W., Lusk, C. H., Niinemets, Ü., Oleksyn, J., Osada, N., Poorter, H., Warton, D. I., and Westoby, M. 2005. Modulation of leaf economic traits and trait relationships by climate. Global Ecology and Biogeography 14: 411421.
Yamada, T., Suzuki, E., and Yamakura, T. 1999. Scaling of petiole dimensions with respect to leaf size for a tropical tree, Scaphium macropodum (Sterculiaceae), in Borneo. Journal of Plant Research 112: 6166.
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