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Palaeo-ecophysiological perspectives on plant responses to global change
REVIEWS 32 Slowinski, J.B. and Ciuyer, C. (1993) Testing whether certain traits have caused amplified diversification: An improved method based on a model of random speciation and extinction, Am. Nar. 142,1019-1024 33 Jensen, J.S.(1990) Plausibility and testability: Assessing the consequences of evolutionary innovation, in Euolutionary Novelties (Nitecki, M.H., ed.), pp. 171-190, University of Chicago Press 34 Doyle, J.A. and Donoghue, M.J. (1993) Phylogenies and angiosperm diversification, fdeobio/ogy 19, 141-167 35 Raikow, R.J. (1986) Why are there so many kinds of passerine birds? Syst. Zoo/. 35,255-259 36 Bulmer, M., Wolfe, K.H. and Sharp, P.M. (1991) Synonymous nucleotide substitution rates in mammalian genes: Implications for the molecular clock and the relationship of mammalian orders, Proc. Nat1 Acad. Sci. USA 88,5974-5978 37 Hasegawa, M., Kishino, H. and Yano, T. (1989) Estimation of branching dates among primates by molecular clocks of nuclear DNA which slowed down in Hominoidea, J. Hum. Euol. 18, 461-476
38 Hasegawa, M., Rienzo, A.D., Kocher, T.D. and Wilson, A.C. (1993) Toward a more accurate time scale for the human mitochondrial DNA tree, J. Mol. Euol. 37, 347-354 39 Walker, T.D. (1985) Diversification functions and the rate of taxonomic evolution, in Phanerozoic Diversity Patterns (Valentine, J.W., ed.), pp. 31 l-334, Princeton University Press 40 Savage, H.M. (1983) The shape of evolution: ‘systematic’ tree topology, Biol. J. Linn. Sot. 20,225-244 41 Huelsenbeck, J.P. and Hillis, D.M. (1993) Success of phylogenetic methods in the four-taxon case, Syst. Biol. 42,247-264 42 Felsenstein, J. (1993) PHYLIP (Phylogeny Inference Package) (Version 3.5~1, J. Felsenstein 43 Bruns, T.D. and Szaro, T.M. (1992) pate and mode differences between nuclear mitochondrbd small-subunit t-RNA genes in mushrooms, Mol. Biol. Eool. 9,836-855 44 Langley, C.H. and Fitch, W.M. (1974) An examination of the constancy of the rate of molecular evolution, J. Mol. Eool. 3, 161-177 45 Nee, S. and Harvey, P.H. (1994) Getting to the roots of flowering plant diversity, Science 264,1549-1550
Palaeo-ecophysiologicalperspectives on plant responsesto global change D.J. Beerling and F.I. Woodward eochemical models of the Taxonomic classifications of plant The second repercussion of large variations in atmospheric long-term carbon cycle species, based on morphological characteristics, provide a stable and CO, is the possible effects on the indicate that the concen1tration of atmospheric carrobust approach for inferring taxonomic ecophysiology of different taxobon dioxide (CO,) has varied greatly and phylogenetlc relationships between nomic plant groups (e.g. ferns, over the course of land plant evoextant and extinct species. This implies cycads, palms, ginkgos and angiolutionl-3. Model results are supthat, although evolution is a continuous sperm and gymnosperm trees) process for a species, there is no that evolved during this time*. ported by analyses of palaeosols4ss and the isotopic composition of whole-scale change in those suites The impact on the photosynthetic fossil porphyrins6 (Fig. 1). The of morphological characteristics that ‘system’ appears to be smalll2; implications of such large CO, varidefine higher order (genus and greater) however, changes in stomata1 ations for plant- atmosphere interrelationships. Recent research suggests physiology and morphology seem that a higher order characteristic very likely - a response that will actions are only now beginning to be explored’-9. stomata1 density - may reflect not only influence the operational range of photosynthesis. Dramatic, long-term CO, changes the atmospheric CO, concentration during have two repercussions for palaeoinitial evolution, but may also strongly In this review, we discuss each ecophysiological research. First, constrain the responses of higher order of these areas in turn. Our apthe observation that leaf stomata1 plant groups to future CO,-enrichment. proach has been to begin with the assemblage of observations of density (number of stomata per unit area of leaf) can be controlled stomata1 density from fossil plants D.J. Beerling and F.I. Woodward are at the Dept of by the concentration of atmosof the late Silurian through to the Animal and Plant Sciences, University of Sheffield, most recent glaciation. Building pheric CO, (Refs 10,ll) offers the Sheffield, UK SlO 2TN. possibility of investigating the relaon these observations from the tionship between stomata1 density fossil record, we then survey the of fossil leaves and CO, on time stomata1 density and photosynscales commensurate with the entire course of land plant thetic characteristics of the ‘early’ evolving plant groups, evolution. lnvestigations of fossil leaves can be used to cycads, palms and ferns growing at the present-day to ask a new question: do major changes in stomata1 density investigate the link with the environmental conditions recorded from fossil leaves correspond to predicted major under which the different taxonomic groups evolved. changes in atmospheric CO, concentration? Estimates of ancient atmospheric CO, changes from observations on fos- Evidence from the palaeobotanical record sil leaves will always be severely limited by the lack of The largest CO, excursion in the geological past (Fig. 1) extant species, which are sometimes needed to calibrate occurred from the Silurian [c. 435 million years ago (Mya)] the relationship between CO, and stomata1 density, and through into the Carboniferous (345-280 Mya) coincident so this approach may only be of use for testing geo- with the evolution of land plants. The stomata1 densities of chemical CO, models and CO, proxies in a semi-quantitative fossilized leaves from these two geological periods are very fashion. markedly different (Fig. 2). Plants growing in the high-CO,
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REVIEWS Devonian atmospherels-15 (e.g. Baragwanathia and Drepanophycus species) had rather low stomata1 densities, typically be tween 28 and 33 mm-z. In contrast, species evolving in the low-CO, Carboniferous period (e.g. Lebachia and Swillingtonia) show very high stomatal densities tovalues of c. 300 and c. 800 mm-z, respectively (Ref. 15) (Fig. 2). The very large increase in stomata1 density from the Lower Devonian to the Carboniferous may be partly attributable to changes in the life form and habitat in which the plants from the different periods grew. However, it could also be fairly argued to be the earliest known stomata1 density response to atmospheric CO, perturbations, which is in accord with the geological CO, data (Fig. 1). The fossil record is only beginning to 100 200 300 400 500 be scrutinized for these types of long-term responses against which geochemical eviYears before present x IO6 dence can be tested, and there is a long gap in the record of stomata1 observations Fig. 1. Geochemical model predictions of long-term changes in the concentration of atmospheric CO, (data from the Carboniferous until the Miocene from Ref. 1, filled circles; Ref. 2, unfilled triangles; Ref. 3, crosses) and reconstructed values from the (26-7 Mya). Miocene fossil leaves of the isotopic composition of fossil porphyrins (chlorophyll derivatives) from deep-ocean cores (Ref. 6, filled genus Quercusspanning the past 10 million triangles) and palaeosols [estimate 1 (Ref. 5) is for a Late Cretaceous (Maastrichtian) paleosol from India giving a single value of 1300 ppm; estimate 2 (Ref. 4) is the range (1500-3000 ppm) for Early Cretaceous years show large variations in stomata1 samples]. density that have been linked to parallel changes in atmospheric CO, and climate recorded from fossil pollen studieG. The well-preserved Miocene-aged fossil conifer needles, from stomata1 density of needles from Miocene representatives the Clarkia formation in Northern Idaho, USA, permit the of Taxodium, Pinus, Cunninghamia and Metasequoia, which measurement of stomata1 charactersir. The difficulties asso- grew in CO, concentrations of 400-800 ppm, are considerciated with the lack of extant species and the possibility of a ably lower than those of extant representatives of the same change in ploidy number’s preclude rigorous comparison genus, by c. 50% (Fig. 2). in terms of a CO, response,‘but nevertheless when such a Detailed morphological studies of fossil leaves focus comparison is made an intriguing response emerges. The attention on the compatibility of ancient CO, proxy indicators and models and the palaeobotanical record. In the Pleistocene, direct measurements of 1200 atmospheric composition of air trapped in ice provide a nearly continuous, but temporally 1000 Acoarse, record of CO, concentra‘E tions for the past 200000 yearsig. 5 800 Consequently, the study of Pleis.i2 tocene fossils switches emphasis E from testing the concordance of % 3 i;j E s cn
600
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400
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SiluroKarbo
Miocene/ present
Glacial (conifer)/ present
Glacial (shrub)/ present
Plant group Fig. 2. Comparison of the stomata1 densities of leaves from fossil plants and from living plants at times of contrasting concentrations of atmospheric CO,. Data sources: Silurian/Lower Devonian plants13814, Carboniferous plantsl5, Miocene conifersl7, glacial-period coniferszz, glacial-period dwarfshrubs20.21. Note that the Silurian/Carboniferous and Miocene/present comparisons are for episodes of high/low CO, and that the glacial/present comparisons are for episodes of low/high CO,.
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Fig. 3. Stomata1 density responses to past changes in atmospheric CO, for temperate angiosperm trees (dashed line) and conifers (solid line). Values are expressed as the percentage of present-day values. Data from Refs 11 and 2.7, respectively.
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REVIEWS Evidence from extant plants The pattern of early angiosperm radiation has been established from extensive analyses of nearly 200 fossil floras of Jurassic, Cretaceous and Palaeocene age23-25.These analyses provide an evolutionary context for the dominant plant groups @teridophytes, cycads, conifers and angiosperms) and show that the first three groups began to make a major contribution to individual late Jurassic floras around 160 million years ago - a time when the geochemical models and other geological proxies predict high CO, concentrations of c. 1000-2000 ppm (Fig. 1). Since palaeo-CO, concentrations have 0 clearly influenced the stomata1 density of I I 1 10 plants that grew in the past (Fig. 2) have 0 500 1000 1500 2000 these leaf morphological characteristics CO, concentration (ppm) been retained by extant representatives of the different plant groups? MeasureFig. 4. Correlation between stomata1 density and CO, compiled from the stomata1 density data of different ments of stomata1 density made on fronds extant plant groups (unfilled symbols) (ferns, cycads, ginkgo, palms) and the approximate CO, concentration1 of ferns, cycads and palms, and leaves under which they were estimated to have evolved, and the data from fossil leaves in Fig. 2 (filled symbols). of ginkgos growing in the University of Sheffield Botanical Gardens, Tapton, show that the species within these ancient the palaeobotanical record and the geochemical evidence groups have 1ow stomata1 densities in the range of and models to a direct attempt to understand how plants re 15-50 mm-z, especially compared to more recently evolved sponded to measured CO, increases from 190 to 300 ppm. angiosperms, trees and grasses. Therefore, these low stomStudies using this approach have shown convincingly that, atal densities are correlated with the palaeo-atmospheric in agreement with experimental observations, leaves of composition under which these different plant groups first dwarf shrubW1 and needles of conifers22 that developed evolved, but the plants have not adapted to the more recent under low full-glacial CO, concentrations (19Oppm) had (in geological terms) CO, decline. more stomata than those that developed under the present It is possible that the evolutionary series we describe or more recent CO, concentration (Fig. 2). might be most strongly explained by changes in the capacity This brief review of data recorded from fossil leaves of the xylem to transport water. However, new ideas on the shows that despite problems associated with the lack of ascent of water26 clearly indicate that xylem conductivity to extant species there is evidence for a marked influence of water is only one aspect in the control of water flow. Therepalaeo-atmospheric composition on leaf morphology. fore, it seems less likely that variations in the structure of the xylem through (evolutionary) times exert the major evolutionary influence on stomata1 density. However, the relation20 ship between xylem conductivity, water transport and stomata1 density clearly requires new analyses, in view of the new developments in plant-water relations. A 15 corollary to the suggestion that some groups of extant plants have retained a stomata1 density reflecting the CO, level under which they formed is that earlier evolving plant groups will be least sensitive to recent CO, increases. The comparative responses of stomata1 density to CO, change of two different-aged plant groups - angiosperm trees” and temperate conifers22- certainly show contrasting Pteridophyte patterns of response consistent with the prediction (Fig. 3). The relationship between CO, and 100 200 300 400 0 stomata1 density can be investigated over the course of geological time by combinPhoton flux (wmol md2 s-l) ing the latest CO, predictions of Berner’si long-term carbon cycle model with the Ftg. 5. The response of leaf photosynthetic rate (A) over a range of irradiances for plants froin different tax@ stomata1 density measurements of fossil nomic groups. Species were: grass, Poa annua; conifer, Picea abies; cycad, Cycas revoluta; pteridophyte, and present-day leaves. These data have Psilotum nudum. Data from Ref. 28. been supplemented by estimating the CO, levels at the time of first appearance of 22
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REVIEWS the plant groups ferns, cycads, palms and ginkgos based on compression fossil flora!+25, and phylogenetic analyses based on the nucleotide sequences of the chloroplastic gene encoding for the large subunit of ribulosal,5-bisphosphate carboxylase/oxygenase (RuBP carboxylase) of extant seed plants27. The results indicate an inverse log-normal relationship between absolute stomata1 density and atmospheric CO, concentration (Fig. 4). Low stomata1 density can limit the supply of CO, into the leaf. In this way, stomata1 density, which has been apparently ‘fixed’ (within the limits of a certain amount of phenotypic plasticity; see Ref. 21) in some early plant groups, may influence leaf gas exchange. This possibility can be tested by investigating the light-response curves of leaf photosynthesis for the different plant groups involved. These light response curves of C3 vascular plants of contrasting taxonomic groups28 show that light-saturated rates of photosynthesis decline in the order pteridophyte
References 1 Berner, R.A. (1994) SGEOCARB II: a revised model of atmospheric CO, over Phanerozoic time, Am. J. Sci. 294,56-91 2 Francois, L.M., Walker, J.C.C.and Opdyke, B. (1993) The history of global weathering and the chemical evolution of the ocean-atmosphere system, Geophys. Monogr 74,143-159 3 Lasaga, AC., Berner, R.A. and Garrells, R.M. (1985) An improved model of atmospheric CO, fluctuations of the past 100 million years,
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Monogr.
32,397-411
4 Cerling, T.E. (1992) The use of carbon isotopes in paleosols as au indicator of the p(COJ of the paleoatmosphere, Global Biogeochem. TREE
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5 Andrews, J.E.,Tandon, S.K.and Dennis, P.F.(1995) Concentrations of carbon dioxide in the Late Cretaceous atmosphere+ J. Gee/. Sot. 152, l-3 6 Freeman, K.H. and Hayes, J.M. (1992) Fractionation of carbon isotopes by phytoplaukton and estimates of ancient CO, levels, Global
Biogeochem.
Cycles 6,185-198
7 Raven, J.A. (1993) The evolution of vascular plants in relation to quantitative functioning of dead water conducting cells and stomata,
Biol. Reu. 68,337-363
8 Beerling, D.J. (1994) Modelling paiaeophotosynthesis: late Cretaceous to present, Philos. Trans. R. Sot. London Ser. B 346, 421-432 9 Robinson, J.M. (1994) Speculations on carbon dioxide starvation, Late Tertiary evolution of stomatal regulation and floristic modernization, Plant Cell Environ. 17,345-354 10 Thomas, J.F. and Harvey, C.N. (1983) Leaf anatomy of four species grown under continuous CO, enrichment, Bat. Gaz. 144, 303-309
11 Woodward, F.I. (1987) Stomatal numbers are sensitive to increases in CO, from pre-industrial levels, Nature 327,617-618 12 Soltis, P.S.,Soltis, D.E. and Smiley, C.J. (1993) An rbcl. sequence fmm a Miocene Tuxodium @aId cypress), Proc. Nat1 Acad. Sci. USA 89,449-451 13 Hueber, F.M. (1983) A new species of Barugwanathia from the sextant formation (Emsian), Northern Ontario, Canada, Bat. J. Linn. Sot. 86,57-79
14 Stubblefield, S. and Banks, H.P. (1978) The cuticle of Drepunophycus spinaformis, long ranging Devonian lycopod from New York and Edstem, Canada, Am. J. Bat. 65,110-l 18 15 McElwain, J. and Chaloner, W.G. Stomatal density and index track atmospheric carbon dioxide changes in the Palaeozoic, Ann. Bot (in press) 16 Van Der Burgh, J., Visscher, H., Dilcher, D.L. and Kiirschner, W.M. (1993) Paleoatmospheric signatures in Neogene fossil leaves, Science
260,1788-1790
17 Huggins, L.M. (1985) Cuticular analyses and preliminary comparisons of some Miocene conifers from Clarkia, Idaho in Late Cenozoic History of the Pacific Northwest (Smiley, C.J.,ed.), pp. 113-138, American Association for the Advancement of Science 18 Masterson, J. (1994) Stomatai size in fossil plants: evidence for polyploidy in majority of Angiosperms, Science 264,421-424 19 Jouzel, J. et al. (1993) Extending the Vostok ice-core record of palaeoclimate to the penultimate glacial period, Nature 364, 407412 20 Beerling, D.J. (1993) Changes in the stomatal density of Eetula nana leaves in response to increase-s in the atmospheric carbon dioxide concentration since the late-glacial, Spec. Pup. Palaeontol. 49,181-187 21 Beerling, D.J. and Chaloner, W.G. (1993) Evolutionary responses of stomatal density to global CO, change, Biol. J. Linn. Sot. 48, 343-353 22 Van De Water, P.K., Leavitt, S.W.and Betancourt, J.L. (1994) Trends in stomatai density and W/WZ ratios of Pinus flexilis needles during last glacial-interglacial cycle, Science
264,239-243
23 Niklas, K.J., Tiffney, B.H. and Knoll, A.H. (1983) Patterns of vascular land plant diversification, Nature 303,614-616 24 Lidgard, S. and Crane, P.R. (1988) Quantitative analyses of the early angiosperm radiation, Nature 331,344-346 25 Knoll, A.H. and Niklas, K.J. (1987) Adaptation, plant evolution, and the fossil record, Rev. Pal. Pal. 50,127-149 26 Zimmerman, U. et al. (1993) Xylem pressure and banspo~? in higher plants and tall trees in Water Deficits: Plant Responses hum Cell lo Community (Smith, J.A.C. and Griffiths, H., eds), pp. 87-108, Bios 27 Savard, L. el al. (1994) Chlomplast and nuclear gene sequences indicate late Pennsylvanian time for the last common ancestor of extant seed plants, Proc. Nat1 Acad. Sci. USA 91,5163-5167 28 Long, S.P.,Postl, W.F. and BolhBr-Nordenkampf, H.R. (1993) Quantum yields for uptake of carbon dioxide in C3 vascular plants of contrasting habitats and taxonomic groupings, Pkmta 189,226-234 29 Golenberg, E.M. el al. (1990) Chioroplast DNA sequence from Miocene Magnolia species, Nature 344,656-658
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38 Hasegawa, M., Rienzo, A.D., Kocher, T.D. and Wilson, A.C. (1993) Toward a more accurate time scale for the human mitochondrial DNA tree, J. Mol. Euol. 37, 347-354 39 Walker, T.D. (1985) Diversification functions and the rate of taxonomic evolution, in Phanerozoic Diversity Patterns (Valentine, J.W., ed.), pp. 31 l-334, Princeton University Press 40 Savage, H.M. (1983) The shape of evolution: ‘systematic’ tree topology, Biol. J. Linn. Sot. 20,225-244 41 Huelsenbeck, J.P. and Hillis, D.M. (1993) Success of phylogenetic methods in the four-taxon case, Syst. Biol. 42,247-264 42 Felsenstein, J. (1993) PHYLIP (Phylogeny Inference Package) (Version 3.5~1, J. Felsenstein 43 Bruns, T.D. and Szaro, T.M. (1992) pate and mode differences between nuclear mitochondrbd small-subunit t-RNA genes in mushrooms, Mol. Biol. Eool. 9,836-855 44 Langley, C.H. and Fitch, W.M. (1974) An examination of the constancy of the rate of molecular evolution, J. Mol. Eool. 3, 161-177 45 Nee, S. and Harvey, P.H. (1994) Getting to the roots of flowering plant diversity, Science 264,1549-1550
Palaeo-ecophysiologicalperspectives on plant responsesto global change D.J. Beerling and F.I. Woodward eochemical models of the Taxonomic classifications of plant The second repercussion of large variations in atmospheric long-term carbon cycle species, based on morphological characteristics, provide a stable and CO, is the possible effects on the indicate that the concen1tration of atmospheric carrobust approach for inferring taxonomic ecophysiology of different taxobon dioxide (CO,) has varied greatly and phylogenetlc relationships between nomic plant groups (e.g. ferns, over the course of land plant evoextant and extinct species. This implies cycads, palms, ginkgos and angiolutionl-3. Model results are supthat, although evolution is a continuous sperm and gymnosperm trees) process for a species, there is no that evolved during this time*. ported by analyses of palaeosols4ss and the isotopic composition of whole-scale change in those suites The impact on the photosynthetic fossil porphyrins6 (Fig. 1). The of morphological characteristics that ‘system’ appears to be smalll2; implications of such large CO, varidefine higher order (genus and greater) however, changes in stomata1 ations for plant- atmosphere interrelationships. Recent research suggests physiology and morphology seem that a higher order characteristic very likely - a response that will actions are only now beginning to be explored’-9. stomata1 density - may reflect not only influence the operational range of photosynthesis. Dramatic, long-term CO, changes the atmospheric CO, concentration during have two repercussions for palaeoinitial evolution, but may also strongly In this review, we discuss each ecophysiological research. First, constrain the responses of higher order of these areas in turn. Our apthe observation that leaf stomata1 plant groups to future CO,-enrichment. proach has been to begin with the assemblage of observations of density (number of stomata per unit area of leaf) can be controlled stomata1 density from fossil plants D.J. Beerling and F.I. Woodward are at the Dept of by the concentration of atmosof the late Silurian through to the Animal and Plant Sciences, University of Sheffield, most recent glaciation. Building pheric CO, (Refs 10,ll) offers the Sheffield, UK SlO 2TN. possibility of investigating the relaon these observations from the tionship between stomata1 density fossil record, we then survey the of fossil leaves and CO, on time stomata1 density and photosynscales commensurate with the entire course of land plant thetic characteristics of the ‘early’ evolving plant groups, evolution. lnvestigations of fossil leaves can be used to cycads, palms and ferns growing at the present-day to ask a new question: do major changes in stomata1 density investigate the link with the environmental conditions recorded from fossil leaves correspond to predicted major under which the different taxonomic groups evolved. changes in atmospheric CO, concentration? Estimates of ancient atmospheric CO, changes from observations on fos- Evidence from the palaeobotanical record sil leaves will always be severely limited by the lack of The largest CO, excursion in the geological past (Fig. 1) extant species, which are sometimes needed to calibrate occurred from the Silurian [c. 435 million years ago (Mya)] the relationship between CO, and stomata1 density, and through into the Carboniferous (345-280 Mya) coincident so this approach may only be of use for testing geo- with the evolution of land plants. The stomata1 densities of chemical CO, models and CO, proxies in a semi-quantitative fossilized leaves from these two geological periods are very fashion. markedly different (Fig. 2). Plants growing in the high-CO,
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REVIEWS Devonian atmospherels-15 (e.g. Baragwanathia and Drepanophycus species) had rather low stomata1 densities, typically be tween 28 and 33 mm-z. In contrast, species evolving in the low-CO, Carboniferous period (e.g. Lebachia and Swillingtonia) show very high stomatal densities tovalues of c. 300 and c. 800 mm-z, respectively (Ref. 15) (Fig. 2). The very large increase in stomata1 density from the Lower Devonian to the Carboniferous may be partly attributable to changes in the life form and habitat in which the plants from the different periods grew. However, it could also be fairly argued to be the earliest known stomata1 density response to atmospheric CO, perturbations, which is in accord with the geological CO, data (Fig. 1). The fossil record is only beginning to 100 200 300 400 500 be scrutinized for these types of long-term responses against which geochemical eviYears before present x IO6 dence can be tested, and there is a long gap in the record of stomata1 observations Fig. 1. Geochemical model predictions of long-term changes in the concentration of atmospheric CO, (data from the Carboniferous until the Miocene from Ref. 1, filled circles; Ref. 2, unfilled triangles; Ref. 3, crosses) and reconstructed values from the (26-7 Mya). Miocene fossil leaves of the isotopic composition of fossil porphyrins (chlorophyll derivatives) from deep-ocean cores (Ref. 6, filled genus Quercusspanning the past 10 million triangles) and palaeosols [estimate 1 (Ref. 5) is for a Late Cretaceous (Maastrichtian) paleosol from India giving a single value of 1300 ppm; estimate 2 (Ref. 4) is the range (1500-3000 ppm) for Early Cretaceous years show large variations in stomata1 samples]. density that have been linked to parallel changes in atmospheric CO, and climate recorded from fossil pollen studieG. The well-preserved Miocene-aged fossil conifer needles, from stomata1 density of needles from Miocene representatives the Clarkia formation in Northern Idaho, USA, permit the of Taxodium, Pinus, Cunninghamia and Metasequoia, which measurement of stomata1 charactersir. The difficulties asso- grew in CO, concentrations of 400-800 ppm, are considerciated with the lack of extant species and the possibility of a ably lower than those of extant representatives of the same change in ploidy number’s preclude rigorous comparison genus, by c. 50% (Fig. 2). in terms of a CO, response,‘but nevertheless when such a Detailed morphological studies of fossil leaves focus comparison is made an intriguing response emerges. The attention on the compatibility of ancient CO, proxy indicators and models and the palaeobotanical record. In the Pleistocene, direct measurements of 1200 atmospheric composition of air trapped in ice provide a nearly continuous, but temporally 1000 Acoarse, record of CO, concentra‘E tions for the past 200000 yearsig. 5 800 Consequently, the study of Pleis.i2 tocene fossils switches emphasis E from testing the concordance of % 3 i;j E s cn
600
-
400
-
SiluroKarbo
Miocene/ present
Glacial (conifer)/ present
Glacial (shrub)/ present
Plant group Fig. 2. Comparison of the stomata1 densities of leaves from fossil plants and from living plants at times of contrasting concentrations of atmospheric CO,. Data sources: Silurian/Lower Devonian plants13814, Carboniferous plantsl5, Miocene conifersl7, glacial-period coniferszz, glacial-period dwarfshrubs20.21. Note that the Silurian/Carboniferous and Miocene/present comparisons are for episodes of high/low CO, and that the glacial/present comparisons are for episodes of low/high CO,.
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Fig. 3. Stomata1 density responses to past changes in atmospheric CO, for temperate angiosperm trees (dashed line) and conifers (solid line). Values are expressed as the percentage of present-day values. Data from Refs 11 and 2.7, respectively.
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REVIEWS Evidence from extant plants The pattern of early angiosperm radiation has been established from extensive analyses of nearly 200 fossil floras of Jurassic, Cretaceous and Palaeocene age23-25.These analyses provide an evolutionary context for the dominant plant groups @teridophytes, cycads, conifers and angiosperms) and show that the first three groups began to make a major contribution to individual late Jurassic floras around 160 million years ago - a time when the geochemical models and other geological proxies predict high CO, concentrations of c. 1000-2000 ppm (Fig. 1). Since palaeo-CO, concentrations have 0 clearly influenced the stomata1 density of I I 1 10 plants that grew in the past (Fig. 2) have 0 500 1000 1500 2000 these leaf morphological characteristics CO, concentration (ppm) been retained by extant representatives of the different plant groups? MeasureFig. 4. Correlation between stomata1 density and CO, compiled from the stomata1 density data of different ments of stomata1 density made on fronds extant plant groups (unfilled symbols) (ferns, cycads, ginkgo, palms) and the approximate CO, concentration1 of ferns, cycads and palms, and leaves under which they were estimated to have evolved, and the data from fossil leaves in Fig. 2 (filled symbols). of ginkgos growing in the University of Sheffield Botanical Gardens, Tapton, show that the species within these ancient the palaeobotanical record and the geochemical evidence groups have 1ow stomata1 densities in the range of and models to a direct attempt to understand how plants re 15-50 mm-z, especially compared to more recently evolved sponded to measured CO, increases from 190 to 300 ppm. angiosperms, trees and grasses. Therefore, these low stomStudies using this approach have shown convincingly that, atal densities are correlated with the palaeo-atmospheric in agreement with experimental observations, leaves of composition under which these different plant groups first dwarf shrubW1 and needles of conifers22 that developed evolved, but the plants have not adapted to the more recent under low full-glacial CO, concentrations (19Oppm) had (in geological terms) CO, decline. more stomata than those that developed under the present It is possible that the evolutionary series we describe or more recent CO, concentration (Fig. 2). might be most strongly explained by changes in the capacity This brief review of data recorded from fossil leaves of the xylem to transport water. However, new ideas on the shows that despite problems associated with the lack of ascent of water26 clearly indicate that xylem conductivity to extant species there is evidence for a marked influence of water is only one aspect in the control of water flow. Therepalaeo-atmospheric composition on leaf morphology. fore, it seems less likely that variations in the structure of the xylem through (evolutionary) times exert the major evolutionary influence on stomata1 density. However, the relation20 ship between xylem conductivity, water transport and stomata1 density clearly requires new analyses, in view of the new developments in plant-water relations. A 15 corollary to the suggestion that some groups of extant plants have retained a stomata1 density reflecting the CO, level under which they formed is that earlier evolving plant groups will be least sensitive to recent CO, increases. The comparative responses of stomata1 density to CO, change of two different-aged plant groups - angiosperm trees” and temperate conifers22- certainly show contrasting Pteridophyte patterns of response consistent with the prediction (Fig. 3). The relationship between CO, and 100 200 300 400 0 stomata1 density can be investigated over the course of geological time by combinPhoton flux (wmol md2 s-l) ing the latest CO, predictions of Berner’si long-term carbon cycle model with the Ftg. 5. The response of leaf photosynthetic rate (A) over a range of irradiances for plants froin different tax@ stomata1 density measurements of fossil nomic groups. Species were: grass, Poa annua; conifer, Picea abies; cycad, Cycas revoluta; pteridophyte, and present-day leaves. These data have Psilotum nudum. Data from Ref. 28. been supplemented by estimating the CO, levels at the time of first appearance of 22
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REVIEWS the plant groups ferns, cycads, palms and ginkgos based on compression fossil flora!+25, and phylogenetic analyses based on the nucleotide sequences of the chloroplastic gene encoding for the large subunit of ribulosal,5-bisphosphate carboxylase/oxygenase (RuBP carboxylase) of extant seed plants27. The results indicate an inverse log-normal relationship between absolute stomata1 density and atmospheric CO, concentration (Fig. 4). Low stomata1 density can limit the supply of CO, into the leaf. In this way, stomata1 density, which has been apparently ‘fixed’ (within the limits of a certain amount of phenotypic plasticity; see Ref. 21) in some early plant groups, may influence leaf gas exchange. This possibility can be tested by investigating the light-response curves of leaf photosynthesis for the different plant groups involved. These light response curves of C3 vascular plants of contrasting taxonomic groups28 show that light-saturated rates of photosynthesis decline in the order pteridophyte
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