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fossil record suggests limited influence of atmospheric CO2 on terrestrial productivity prior to angiosperm

C. Kevin Boycea,1 and Maciej A. Zwienieckib,c

aDepartment of the Geophysical Sciences, University of Chicago, Chicago, IL 60637; bArnold Arboretum of Harvard University, Boston, MA 02131; and cDepartment of Sciences, University of California, Davis, CA 95616

Edited by Andrew H. Knoll, Harvard University, Cambridge, MA, and approved May 18, 2012 (received for review March 5, 2012)

Declining CO2 over the Cretaceous has been suggested as an evo- complications. For example, it is in conflict with a variety of hy- − lutionary driver of the high leaf vein densities (7–28 mm mm 2) potheses regarding the angiosperm radiation that are dependent that are unique to the angiosperms throughout all of Earth his- on high productivity being unique to the flowering and tory. Photosynthetic modeling indicated the link between high not a general trait of all plants in a high-CO2 world (19–22). vein density and productivity documented in the modern low- Furthermore, if productivity were highly CO2-dependent, that CO2 regime would be lost as CO2 concentrations increased but also dependence would carry through even to the availability of dif- implied that plants with very low vein densities (less than 3 mm ferent architectural and ecological possibilities. For example, − mm 2) should experience substantial disadvantages with high occupation of frequently disturbed habitats requires high enough CO2. Thus, the hypothesized relationship between CO2 and plant productivity to complete a life cycle between successive distur- evolution can be tested through analysis of the concurrent histo- bance events (23); thus, the accessibility of disturbed habitats ries of alternative lineages, because an extrinsic driver like atmo- as a viable environment would have fluctuated tremendously fl spheric CO2 should affect all plants and not just the owering through time for all plant lineages. Finally, if the correlation plants. No such relationship is seen. Regardless of CO2 concentra- between CO2 concentrations and productivity is tightly and tions, low vein densities are equally common among nonangio- strongly positive, that would even have an impact on our under- sperms throughout history and common enough to include standing of atmospheric CO2 itself, because the standard mod- forest canopies and not just obligate shade species that will al- eling of vegetation, atmospheric, and geological processes to ways be of limited productivity. Modeling results can be reconciled determine CO2 concentrations includes only modest increases in with the fossil record if maximum assimilation rates of nonflow- productivity as CO2 increases. The temporal variability of CO2 ering plants are capped well below those of flowering plants, would be dampened if CO2 fertilization effects were greater capturing biochemical and physiological differences that would because of the feedbacks of the additional plant productivity on be consistent with extant plants but previously unrecognized in CO2 drawdown through increased silicate weathering (figure 10 the fossil record. Although previous photosynthetic modeling sug- in ref. 24). Paradoxically, the models of plant function suggesting gested that productivity would double or triple with each Phaner- that large swings in productivity accompany the large changes in ozoic transition from low to high CO , productivity changes are 2 CO2 concentrations would also make those large changes in CO2 likely to have been limited before a substantial increase accompa- difficult to achieve because of these feedbacks. nying the evolution of flowering plants. Models of plant function in the geological past are difficult to test experimentally because modern plants have evolved under paleoecology | | tracheophyte low-CO2 conditions and greenhouse tests at elevated CO2 levels cannot be carried out over macroevolutionary time scales (15), but a solution may be available for the testing of their accuracy and Role of CO2 in Plant Evolution and Productivity over completeness by comparing predictions against the fossil record. Geological Time Scales Here, we use leaf fossils to test morphological predictions derived fl tmospheric CO2 concentrations have uctuated greatly over from models of plant function under elevated CO2 regimes to fl Athe past 400 million years: CO2 levels are thought to have evaluate previous hypotheses regarding the role of CO2 uctua- decreased by a factor of 10 or more as a result of the Devonian tions in driving angiosperm evolution and primary productivity. evolution of deep rooting plants and, subsequently, to have

varied between levels somewhat less than and fivefold greater Leaf Vein Density EVOLUTION than preindustrial levels (1, 2). Just as land plant evolution has The high density of veins found in the of many flowering been a primary driver of these changes, in turn, CO2 has often plants is unique. Nonangiosperms average about 2.5 mm of vein been assigned a dominant role in plant evolution. CO2 changes length per square millimeter of leaf area and rarely reach higher − − have been implicated for the radiation of vascular plants, than 5 mm mm 2, but angiosperms average around 10 mm mm 2 −2 plants, and flowering plants; for the spread of C4 photosynthesis and can reach higher than 25 mm mm , with high vein densities and grasslands; and for the evolution of arborescence and both appearing independently in at least three angiosperm lineages: laminate leaves in general and the high vein density leaves of the magnoliids, monocots, and eudicots (14, 25, 26). This abun- angiosperms in particular (3–12). Furthermore, models of plant dance of vasculature was shown to correlate with much higher SCIENCES function have repeatedly predicted that large swings in terrestrial ENVIRONMENTAL productivity of 200–300% accompany these changes in atmo- spheric CO2 (13–16). Author contributions: C.K.B. and M.A.Z. designed research; C.K.B. and M.A.Z. performed research; C.K.B. and M.A.Z. analyzed data; and C.K.B. and M.A.Z. wrote the paper. Plants require CO2, and productivity can be adversely affected fl by the CO2 minima of the recent geological past that have The authors declare no con ict of interest. approached the CO2 compensation point for plant growth (17, This article is a PNAS Direct Submission. 18), but did the positive relationship with CO2 carry to a dou- 1To whom correspondence should be addressed. E-mail: [email protected]. bling or tripling of current productivity during the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. highs in CO2 concentration? This suggestion raises a number of 1073/pnas.1203769109/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1203769109 PNAS | June 26, 2012 | vol. 109 | no. 26 | 10403–10408 Downloaded by guest on September 26, 2021 physiological activity, including a fourfold increase in transpira- because only moderate gains in assimilation rate accompany tion capacity and more than a doubling of assimilation capacity, increasing vein density, this should not be expected in a world of −2 that resulted in important implications both for tropical climate 1,000 ppm CO2, where plants with a vein density of 2 mm mm and vegetation feedbacks and for the rise to ecological domi- were modeled to assimilate almost twice as fast as plants with − nance of angiosperms over the Cretaceous and early Paleocene a vein density of 1 mm mm 2 (figure S4 in ref. 14). This modeling – (14, 27 29). However, those correlations of leaf vein density with of plant function in high CO2 thus suggests that an absolute and assimilation capacities are based on empirical difference in assimilation capacities as large as that between measurements of living plants grown under the low ambient CO2 modern and angiosperm tropical and crops would be concentrations of the modern world (14, 25, 30). compressed between two vein densities that would both be ex- Modeling of leaf physiology at the 1,000-ppm CO2 concen- ceedingly low by modern angiosperms. This range of very low trations that are believed to have been exceeded during the vein densities is equally achievable by any lineage of vascular Cretaceous suggests that nearly all plants would have been much plants and in any environment: High vein densities may require more productive than they are today (13–15) and that the ad- ample water supply, but low vein densities are available any- vantage of increased vein density would saturate at low vein where from the rainforest understory to desert succulents. density levels that are accessible by all plant groups (14) (results Testing the hypothesized relationship between CO2 and an- reproduced in Fig. 1B). Thus, it has been argued that the Cre- giosperm leaf evolution is complicated by high leaf vein density taceous initiation of an overall trend in atmospheric CO2 re- being unique to the angiosperms; however, all other plants duction toward modern levels was essential for the emergence of should respond similarly within their potential range even if they angiosperm leaf characteristics because high vein density pro- lack the developmental and physiological capacities for the very vides no advantage with high CO2 (14). high vein densities exhibited by angiosperms. Thus, at times of Emphasis has been on the lack of advantage for high vein high CO2 when very low vein densities should be maladaptive, density in a high-CO2 world (14), but perhaps the more important few fossil leaves should have had vein densities less than 3 mm − conclusion to draw from this physiological model is that possession mm 2 regardless of phylogenetic affinity. − of leaf vein densities much lower than 3 mm mm 2 would present enormous disadvantages because it is associated with dramatic loss Results and Discussion of CO2 assimilation capabilities. Although the modern low-CO2 Fossil History of Leaf Vein Densities. When leaf fossils are sampled world can be permissive of a broad morphological diversity from high-CO2 intervals, the prediction of decreasing prevalence

Fig. 1. Expected relationships between vein density and assimilation capacity and fossil leaf vein density distributions relative to CO2 concentrations. (A) Comparison of empirical measurements (circles) of relation between leaf vein density and stomatal conductance [digitized from the study by Brodribband Feild (14)], with alternative models relating vein density and assimilation capacities, including a previously used model with fixed leaf thickness (14) and a previously undescribed corrected model allowing thickness to vary with vein density (36). (B) Modeled effects of vein density on assimilation capacities at

high (1,000 ppm) and low (350 ppm) atmospheric CO2 concentrations for uncorrected and vein density/leaf thickness-corrected models. (C) Photosynthetic rate gain for change in vein density at high and low CO2 calculated with the corrected model. (D) Distribution of vein densities at different times in Earth history plotted at GEOCARBIII (24) and GEOCARBSULF (55) estimates of contemporaneous CO2. Myr, million years. Specific data are provided in Table S1.

10404 | www.pnas.org/cgi/doi/10.1073/pnas.1203769109 Boyce and Zwieniecki Downloaded by guest on September 26, 2021 − of low vein densities below 3 mm mm 2 proves to be false (Table S1; full ANOVA statistical results are provided in SI Text). Vein densities change little through time, and high proportions of nonangiosperms have vein densities lower than this threshold throughout Earth history and over a wide range of CO2 con- centrations (Fig. 1D). This abundance of low vein density leaves is too great to be accounted for by plants that are independently constrained to low productivity by deep shade or other envi- ronmental stressors. First, the vein densities in question are low regardless of environment: Shade-requiring angiosperms can − have vein densities greater than 5 mm mm 2 (26). More gener- ally, the paleobotanical record is biased toward preservation of woody plants of forest canopies and more open environments because herbs and of the shaded forest floor produce fewer leaves and their leaves have less opportunity for transport to waterway-based sites of deposition and are more prone to decay (31, 32). The cases in which all plants are preserved equally are rare (33, 34). Thus, a few of the lower bound outliers of vein density may well represent tolerators of deep shade, but the vein density for each time interval is sometimes less − − than 2 mm mm 2 and is never more than 2.6 mm mm 2 for each high-CO2 time interval (Fig. 1D). Thus, if more than 50% of the taxa have very low vein densities, it can be safely inferred that a high proportion of the canopy plants had such vein densities. Furthermore, the bias toward preservation of plants growing along lakes and rivers that has been problematic for leaf-based paleoclimate proxies (35) does not explain the prevalence of low vein density plants through time because riparian and non- riparian plants have similar vein densities (Fig. S1 and Table S2). Our results indicate that plants with very low densities grew side by side with plants of higher vein density regardless of CO2 concentrations, contrary to the prediction that those plants would be subject to enormous disadvantages when atmospheric CO2 was high. Fig. 2. Impact on assimilation of stomatal conductance and atmospheric oxygen. (A) Changes in predicted assimilation rate in relation to vein density Reconciling Physiology and the Fossil Record. The prediction de- caused by introducing decreased stomatal conductance in response to high-

rived from physiological modeling that very low leaf vein densi- CO2 concentrations (16) and/or changes attributable to the elevated O2 ties should be rare during times of elevated CO2 is not met by the concentrations expected for the Cretaceous (52, 55) applied to the model fossil record, and no trivial correction is available to bring these corrected for leaf thickness. (B) Photosynthetic rate gain for change in vein two approaches into concordance (full details on model correc- density as predicted for inclusion of model corrections for stomatal con- tions are provided in SI Text). First, the original model (14) only ductance and O2 concentrations. gs, stomatal conductance to water allowed for very thin leaves, which is adequate only for high vein densities. The distance between veins should roughly equal the The steep disadvantages to very low vein density suggested by distance from vein to stomata for optimal water delivery (36), such that low vein density plants in exposed environments would photosynthetic models derive from the assumption that given require much thicker leaves to avoid partial desiccation of the enough CO2, any exposed to adequate light could be more fl leaf lamina. A more accurate scaling of leaf thickness to vein productive than angiosperm crops, such as sun ower or maize, fi density provides a better fit to experimental data (Fig. 1A), but are now with modern CO2 concentrations (e.g., gure S4 in ref. this more accurate depiction increases the distance of high-re- 14). Only lower maximum assimilation rates for nonangiosperms sistance hydraulic transport through the mesophyll in low vein could explain the lack of a correlation between vein density and

density leaves, and thereby accentuates their potential dis- CO2 concentration: A lower plateau for assimilation capacities EVOLUTION advantages (Fig. 1 B and C). Second, although poorly con- would also lower the vein density at which that plateau is ach- strained, stomatal conductivity should have been lower with the ieved, potentially encompassing the entire range of available vein reduced stomatal density seen at times of high CO2 in the geo- densities (Fig. 4 A and B). Vein density would then be free to – logical past (37 40). Reducing stomatal conductivity does in- vary in response to environmental and ecological specialization crease the vein density at which productivity plateaus but without with little impact on assimilation capacities. altering the overall conclusion that the penalty of low vein In this scenario, angiosperms would have advantages over density is far larger when CO is high (Fig. 2). Third, the O /CO 2 2 2 other plant groups regardless of CO concentration, as would be SCIENCES ratio can have an impact on maximum photosynthetic rates 2 consistent with other differences in angiosperm vegetative bi- ENVIRONMENTAL through photorespiration, but elevated oxygen does not alter ology, including leaf traits and stomatal conductivity through expectations (Fig. 2), and neither does consideration of a more time (16, 25, 41–43). In the modern low-CO2 world, individual complete range of potential CO2 concentrations (Fig. 3). The expectation would remain that very low vein densities should be nonangiosperms, particularly some conifers, can overlap with less productive flowering plants, but both the typical and maxi- strongly disfavored during high-CO2 regimes because even small increases in the vein density would dramatically improve pho- mum photosynthetic capacities of angiosperms are substantially tosynthetic capacity (Fig. 3), an expectation rejected by the fossil higher (42–45). Although it is always unclear how literally such record even though these small changes would be equally experiments should be extrapolated up to macroevolutionary available to all plant lineages. time scales, angiosperm advantages do persist and substantial

Boyce and Zwieniecki PNAS | June 26, 2012 | vol. 109 | no. 26 | 10405 Downloaded by guest on September 26, 2021 Fig. 3. Model expectations for the relationship between productivity and

the full range of potential leaf vein densities and CO2 concentrations. Modern O2 concentrations, as well as corrections to the original model for variable leaf thickness and stomatal conductance, were used.

lineage-specific differences in CO2 fertilization are seen when modern plants are exposed to 1,000 ppm CO2 (Fig. 4C). Further support for physiological distinctions between angio- sperms and other plants is that angiosperm leaf fossils do con- form to the model expectations that nonangiosperms violate. The earliest angiosperms share the same range of very low vein densities as nonangiosperms; however, as they evolve the higher vein densities indicative of higher photosynthetic capacities over the high-CO2 Late Cretaceous, they also vacate the vein densities − less than 3 mm mm 2 in a way that is not seen among non- angiosperms (figure 1 in ref. 26), where very low vein densities account for almost 50% of angiosperms in the pre-Albian Early Cretaceous, 7% in the Albian, and no more than 4% in the Late Cretaceous and Paleocene. This provides additional evidence Fig. 4. Impact of maximum rate of Rubisco carboxylation, V ,onassimi- that the patterns seen among nonangiosperm leaf fossils cannot cmax lation capacity at 1,000 ppm of CO2.(A) For the fully corrected model, changes be dismissed as an artifact of the perpetual existence of plants in predicted assimilation rate in relation to vein density are shown for dif- −2 −1 environmentally limited to low productivity. Any such ecological ferent values of Vcmax (μmol·m ·s ). (B)Photosyntheticrategainwith caveat should have applied equally to the angiosperm record, changing vein density for different values of Vcmax.(C) Empirical measurement particularly because obligate shade plants are both ancestral and of lineage-specific relationships between vein density and assimilation at 1,000 continuously abundant for angiosperms (46). ppm of CO2 in living ferns, , and angiosperms plotted along Although modeled in terms of limitations on the maximum rate with modeled relationships between vein density and assimilation capacity at of carboxylation, actual lineage-specific limitations on maximum two Vcmax levels. Amax, light-saturated photosynthesis. A plant species list is photosynthetic capacity could take any number of forms. Rubisco provided in Table S3. activity is well known as a CO2-dependent limit on photosynthesis that suggests highly elevated productivity as CO2 increases (5, 15, available before angiosperm evolution. Previous workers have 47). However, other limitations provide more opportunity for been careful to acknowledge that those values are maxima that fi lineage-speci c differences that are much less CO2-dependent, may not be reached because of other limitations, such as water such as investment in photoreceptors or the Calvin cycle re- availability. However, those elevated levels of productivity are generation of RuBP (47, 48), or may actually be exacerbated by reached by flowering plants in many extant environments, in- increasing CO2, such as the nitrate assimilation (49) and inorganic cluding rainforests and more temperate environments where phosphate recycling that are also necessary for primary pro- moisture is adequate (14), and we argue no plant could achieve duction (48, 50). Without constraining which factors may be in- those levels seen in the modern world before the advent of volved, the stability of vein density distributions throughout the angiosperms regardless of CO2 concentrations. fossil record outside of the angiosperms suggests substantially lower photosynthetic capacities in most nonangiosperms regard- Plant Productivity Through Time and Environmental Implications. If less of CO2 concentrations. Rather than productivity potentially most nonangiosperms do indeed have limited capacity for as- − − ranging from 10 to more than 40 μmol·m 2s 1 through time (13, similation much greater than their modern levels, the large 15), no more than the bottom half of that range may have been swings in productivity through time predicted by modeling

10406 | www.pnas.org/cgi/doi/10.1073/pnas.1203769109 Boyce and Zwieniecki Downloaded by guest on September 26, 2021 vegetation responses to CO2 are unlikely to have happened, stomatal conductivity, the lower internal CO2 concentrations except for a potential increase over the Cretaceous and Cenozoic that might be expected to accompany higher assimilation rates with the spread of angiosperms. This would be more consistent would decrease isotopic discrimination, but internal CO2 con- with carbon cycle modeling than the doubling or tripling of as- centrations might not have been lower if angiosperm hydraulic similation rates that has been predicted with elevated CO2 and modifications allowed stomata to be open a greater proportion fi would have been likely to prevent elevated CO2 in the rst place of the time. Increased Cretaceous abundance of charcoal has through silicate weathering feedbacks. This hypothesis of relative been argued to reflect increased angiosperm assimilation rates stability for plant productivity through history at and fuel production (20), although over longer time periods, least up to the Cretaceous would be an important grounding for charcoal abundance has been considered more as an indicator of consideration of the evolution of terrestrial animals and eco- atmospheric oxygen levels than of plant productivity (20, 52, 53). systems. Contradictory views of how productivity has changed Tests resulting from plant paleoecology may be the most in- since the Cretaceous exist in the literature (8, 13–16, 19–22, 25). fl fl formative. Of all plant growth forms, annuals are the most de- Have owering plants brought ourishing abundance that also pendent on high growth rates. If productivity was tightly benefited animal life (perhaps even in the oceans), or are correlated with CO concentrations, this might be expected to angiosperms simply the best at enduring the deprivations of 2 carry over to the abundance and diversity of annual plants a diminished, carbon-starved world? Consideration of photo- through time as well. Annuals are effectively absent outside of synthetic models in light of the fossil record suggests that pro- ductivity has not declined with angiosperm evolution and is likely the angiosperms throughout earth history (54), regardless of to have increased. CO2 concentrations. The potential of increased productivity with angiosperm evo- Materials and Methods lution is bolstered by a final discrepancy between model output and : Although flowering plant leaf vein densi- All vein density measurements were performed with ImageJ (National − − ties average around 10 mm mm 2 and can surpass 25 mm mm 2, Institutes of Health). Extant leaf vein density measurements were performed on a minimum of five leaves for each taxon. Fossil leaf vein density was photosynthetic models suggest there is never an advantage to fi −2 measured from individual gured specimens or compiled from previously densities greater than about 8 mm mm regardless of CO2 published studies (details are provided in Table S1). Angiosperm vein density concentrations. This expectation is based on the modeling of measurements were based on three subsamples of each leaf at a magnifi- maximum instantaneous assimilation rates dependent on the cation of 20× to 40×; however, this is not necessary for the thick veins and maximum flux of CO2 through the stomata when they are open. lower vein densities of nonflowering plants, for which the vein density of Along with other aspects of angiosperm hydraulic physiology, the entire lamina was measured. The photosynthetic model was derived such as vessels and reduced safety margins (51), high vein densities from a previous source (14) with some corrections of parameter values as − greater than 10 mm mm 2 may instead be important for maxi- explained in SI Materials and Methods. Empirical measurements of photo- mizing the proportion of stomata that are not closed. Thus, the synthetic rates in living plants were collected using a photosynthesis mea- expectation is further bolstered that angiosperms have productivity suring system (LiCor 6400; with photosynthetically active radiation = 2,000 μE and CO concentration = 1,000 ppm; leaves were allowed 20 min of acclima- advantages over other plants whether CO2 is high or low. 2 Future tests regarding changes in productivity through time tion time in the chamber before measurements). with CO2 fluctuations and angiosperm evolution may be chal- ACKNOWLEDGMENTS. We thank Joe , Dana Royer, Patrick MacGuire, lenging but could come from a variety of directions. Increased and Michael Foote for helpful discussion or recitation. This work was photosynthetic capacities in angiosperms may not have had much supported by National Science Foundation Grant EAR-1024041 (to C.K.B. impact on the carbon isotopic values of plants: For a given and M.A.Z.).

1. Beerling DJ, Berner RA (2005) Feedbacks and the coevolution of plants and atmo- 17. Pagani M, Caldeira K, Berner RA, Beerling DJ (2009) The role of terrestrial plants in

spheric CO2. Proc Natl Acad Sci USA 102:1302–1305. limiting atmospheric CO(2) decline over the past 24 million years. Nature 460:85–88. 2. Berner RA (1997) The rise of plants and their effect on weathering and atmospheric 18. Ward JK, et al. (2005) Carbon starvation in glacial trees recovered from the La Brea tar

CO2. Science 276:544–546. pits, southern California. Proc Natl Acad Sci USA 102:690–694. 3. Barrett PM, Willis KJ (2001) Did dinosaurs invent flowers? Dinosaur-angiosperm co- 19. Bond WJ (1989) The tortoise and the hare: Ecology of angiosperm dominance and evolution revisited. Biol Rev Camb Philos Soc 76:411–447. persistence. Biol J Linn Soc Lond 36:227–249. 4. Becker P (2000) Competition in the regeneration niche between conifers and an- 20. Bond WJ, Scott AC (2010) Fire and the spread of flowering plants in the Cretaceous. giosperms: Bond’s slow seedling hypothesis. Funct Ecol 14:401–412. New Phytol 188:1137–1150.

5. Beerling DJ (2005) A History of Atmospheric CO2 and Its Effects on Plants, Animals, 21. Vermeij GJ, Grosberg RK (2010) The great divergence: When did diversity on land and Ecosystems, eds Ehleringer JR, Cerling TE, Dearing MD (Springer, New York), pp exceed that in the sea? Integr Comp Biol 50:675–682. 114–132. 22. Vermeij GJ (2011) The energetics of modernization: the last 100 million years of biotic 6. Beerling DJ, Osborne CP, Chaloner WG (2001) Evolution of leaf-form in land plants evolution. Paleontological Res 15:54–61. EVOLUTION linked to atmospheric CO2 decline in the Late Palaeozoic era. Nature 410:352–354. 23. Grime JP (2002) Plant Strategies, Vegetation Processes, and Ecosystem Properties 7. Cerling TE, et al. (1997) Global vegetation change through the Miocene/Pliocene (Wiley, Hoboken, NJ).

boundary. Nature 389:153–158. 24. Berner RA, Kothavala Z (2001) GEOCARB III: A revised model of atmospheric CO2 over

8. McElwain JC, Willis KJ, Lupia R (2005) A History of Atmospheric CO2 and Its Effects on Phanerozoic time. Am J Sci 301:182–204. Plants, Animals, and Ecosystems, eds Ehleringer JR, Cerling TE, Dearing MD (Springer, 25. Boyce CK, Brodribb TJ, Feild TS, Zwieniecki MA (2009) Angiosperm leaf vein evolution New York), pp 133–166. was physiologically and environmentally transformative. Proc Biol Sci 276:1771–1776. 9. Osborne CP, Beerling DJ, Lomax BH, Chaloner WG (2004) Biophysical constraints on 26. Feild TS, et al. (2011) Fossil evidence for Cretaceous escalation in angiosperm leaf vein the origin of leaves inferred from the fossil record. Proc Natl Acad Sci USA 101: evolution. Proc Natl Acad Sci USA 108:8363–8366. 10360–10362. 27. Boyce CK, Lee J-E (2010) An exceptional role for flowering in the SCIENCES 10. Robinson JM (1994) Speculations on carbon dioxide starvation, late Tertiary evolution expansion of tropical rainforests and . Proc Biol Sci 277:3437–3443. of stomatal regulation and floristic modernization. Environ 17:345–354. 28. Boyce CK, Lee J-E, Feild TS, Brodribb T, Zwieniecki MA (2010) Angiosperms helped put ENVIRONMENTAL 11. Willis KJ, McElwain JC (2002) The Evolution of Plants (Oxford Univ Press, Oxford). the rain in the rainforests: The impact of plant physiological evolution on tropical 12. Woodward FI (1998) Do plants need stomata? J Exp Bot 49:471–480. biodiversity. Ann Mo Bot Gard 97:527–540. 13. Beerling DJ, Woodward FI (1997) Changes in land plant function over the Phanero- 29. Lee J-E, Boyce CK (2010) Impact of the hydraulic capacity of plants on water and zoic: Reconstructions based on the fossil record. Bot J Linn Soc 124:137–153. carbon fluxes in tropical South America. J Geophys Res 115:D23123. 14. Brodribb TJ, Feild TS (2010) Leaf hydraulic evolution led a surge in leaf photosynthetic 30. Brodribb TJ, Feild TS, Jordan GJ (2007) Leaf maximum photosynthetic rate and ve- capacity during early angiosperm diversification. Ecol Lett 13:175–183. nation are linked by hydraulics. Plant Physiol 144:1890–1898.

15. Franks PJ, Beerling DJ (2009) CO(2)-forced evolution of plant gas exchange capacity 31. Ferguson DK (1985) The origin of leaf-assemblages- new light on an old problem. Rev and water-use efficiency over the Phanerozoic. Geobiology 7:227–236. Palaeobot Palynol 46:117–188.

16. Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on sto- 32. Spicer RA (1991) Taphonomy: Releasing the Data Locked in the Fossil Record, eds matal size and density over geologic time. Proc Natl Acad Sci USA 106:10343–10347. Allison PA, Briggs DEG (Plenum, New York), Vol 9, pp 71–113.

Boyce and Zwieniecki PNAS | June 26, 2012 | vol. 109 | no. 26 | 10407 Downloaded by guest on September 26, 2021 33. Wang J, Pfefferkorn HW, Zhang Y, Feng Z (2012) Permian vegetational Pompeii from 44. Wullschleger SD (1993) Biochemical limitations to carbon assimilation in C3 plants—A Inner Mongolia and its implications for landscape paleoecology and paleobiogeog- retrospective analysis of the A/Ci curves from 109 species. J Exp Bot 44:907–920. raphy of Cathaysia. Proc Natl Acad of Sci USA 109:4927–4932. 45. Zhang S, Dang Q-L (2005) Effects of soil temperature and elevated atmospheric CO2 34. Wing SL, Hickey L J, Swisher CC (1993) Implications of an exceptional fossil flora for concentration on gas exchange, in vivo carboxylation and fluorescence in Late Cretaceous vegetation. Nature 363:342–344. jack pine and white birch seedlings. Physiol 25:523–531. 35. Burnham RJ, Pitman NCA, Johnson KR, Wilf P (2001) Habitat-related error in esti- 46. Feild TS, Arens NC, Doyle JA, Dawson TE, Donoghue MJ (2004) Dark and disturbed: A mating temperatures from leaf margins in a humid tropical forest. Am J Bot 88: new image of early angiosperm ecology. Paleobiology 30:82–107. 1096–1102. 47. Long SP, Bernacchi CJ (2003) Gas exchange measurements, what can they tell us 36. Noblin X, et al. (2008) Optimal vein density in artificial and real leaves. Proc Natl Acad about the underlying limitations to photosynthesis? Procedures and sources of error. Sci USA 105:9140–9144. J Exp Bot 54:2393–2401.

37. Beerling DJ, Chaloner WG (1994) Atmospheric CO2 changes since the last glacial 48. Stitt M (1986) Limitation of photosynthesis by carbon metabolism: I. Evidence for maximum: Evidence from the stomatal density record of fossil leaves. Rev Palaeobot excess electron transport capacity in leaves carrying out photosynthesis in saturating

Palynol 81:11–17. light and CO2. Plant Physiol 81:1115–1122. 38. McElwain JC (1998) Do fossil plants signal palaeoatmospheric CO2 concentration in 49. Bloom AJ, Burger M, Rubio Asensio JS, Cousins AB (2010) Carbon dioxide enrichment the geological past? Philos Trans R Soc Lond B Biol Sci 353:83–96. inhibits nitrate assimilation in wheat and Arabidopsis. Science 328:899–903.

39. McElwain JC, Chaloner WG (1995) Stomatal density and index of fossil plants track 50. Sage RF (1994) Acclimation of photosynthesis to increasing atmospheric CO2: The gas atmospheric carbon dioxide in the Paleozoic. Ann Bot (Lond) 76:389–395. exchange perspective. Photosynth Res 39:351–368. 40. Royer DL (2001) Stomatal density and stomatal index as indicators of paleoatmo- 51. Brodribb TJ, Holbrook NM (2004) Stomatal protection against hydraulic failure: A

spheric CO(2) concentration. Rev Palaeobot Palynol 114:1–28. comparison of coexisting ferns and angiosperms. New Phytol 162:663–670. 41. Ida K (1981) Eco-physiological studies on the response of taxodiaceous conifers to 52. Belcher CM, McElwain JC (2008) Limits for combustion in low O2 redefine paleo- shading, with special reference to the behavior of leaf pigments. 1. Distribution of atmospheric predictions for the Mesozoic. Science 321:1197–1200. carotenoids in green and autumnal reddish brown leaves of gymnosperms. Bot Mag 53. Scott AC, Glasspool IJ (2006) The diversification of Paleozoic fire systems and fluc- Tokyo 94:41–54. tuations in atmospheric oxygen concentration. Proc Natl Acad Sci USA 103:10861– 42. Karst AL, Lechowicz MJ (2007) Are correlations among foliar traits in ferns consistent 10865. with those in the seed plants? New Phytol 173:306–312. 54. Boyce CK, Leslie AB The paleontological context of angiosperm vegetative evolution. 43. Ripullone F, Grassi G, Lauteri M, Borghetti M (2003) Photosynthesis-nitrogen rela- Int J Plant Sci, in press.

tionships: Interpretation of different patterns between Pseudotsuga menziesii and 55. Berner RA (2006) GEOCARBSULF: A combined model for Phanerozoic atmospheric O2 Populus x euroamericana in a mini-stand experiment. Tree Physiol 23:137–144. and CO2. Geochim Cosmochim Acta 70:5653–5664.

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