Important Lessons for Species to Biomes from Vegetation Responses to Past Global Change

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Annual Review of Plant Biology Paleobotany and Global Change: Important Lessons for Species to Biomes from Vegetation Responses to Past Global Change

Jennifer C. McElwain

Botany Department, Trinity College Dublin, The University of Dublin, Dublin 2, Ireland; email: [email protected]

Annu. Rev. Plant Biol. 2018. 69:761–87 Keywords The Annual Review of Plant Biology is online at CO2, polar ampliﬁcation, migration, adaptation, resilience, leaf traits, plant.annualreviews.org extinction, leaf mass per area, paleoclimate, paleoatmosphere https://doi.org/10.1146/annurev-arplant-042817- 040405 Abstract Copyright c 2018 by Annual Reviews. Human carbon use during the next century will lead to atmospheric car- All rights reserved bon dioxide concentrations ( pCO2) that have been unprecedented for the past 50–100+ million years according to fossil plant-based CO2 estimates. The paleobotanical record of plants offers key insights into vegetation re- ANNUAL REVIEWS Further sponses to past global change, including suitable analogs for Earth’s climatic

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org Click here to view this article's future. Past global warming events have resulted in transient poleward mi- online features: Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. • Download ﬁgures as PPT slides gration at rates that are equivalent to the lowest climate velocities required • Navigate linked references for current taxa to keep pace with climate change. Paleobiome reconstruc- • Download citations • Explore related articles tions suggest that the current tundra biome is the biome most threatened • Search keywords by global warming. The common occurrence of paleoforests at high polar

latitudes when pCO2 was above 500 ppm suggests that the advance of woody shrub and tree taxa into tundra environments may be inevitable. Fossil pollen studies demonstrate the resilience of wet tropical forests to global change

up to 700 ppm CO2, contrary to modeled predictions of the future. The paleobotanical record also demonstrates a high capacity for functional trait evolution as an additional strategy to migration and maintenance of a species’ climate envelope in response to global change.

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Contents INTRODUCTION ...... 762 GEOLOGICAL CONTEXT FOR CONTEMPORARY GLOBAL CHANGE . . . . . 762 VASCULARPLANTSANDATMOSPHEREEVOLUTION...... 763 THE FOSSIL PLANT RECORD AND PAST GLOBAL CHANGE ...... 764 POLAR AMPLIFICATION AND PAST VEGETATION RESPONSES ...... 770 PAST GLOBAL CHANGE AND IMPACTS ON PLANT COMMUNITYCOMPOSITION...... 771 Extinction, Migration, and Past Global Change ...... 772 Paleobotany, Adaptation, and Past Global Change...... 773 TheEnd-TriassicMassExtinctionEvent...... 773 Case Study of Past Global Change: Astartekløft, East Greenland ...... 775 TRAITADAPTATIONANDPHYSIOLOGICALFEEDBACK...... 776

PALEOBOTANICAL INSIGHTS ON CO2 FERTILIZATION OFPHOTOSYNTHESIS...... 777

INTRODUCTION Paleobotany is the study of fossil plants in deep geological time. It is concerned with the history of the Earth’s vegetation on evolutionary time scales, encompassing on a global scale both long periods of relative climatic stability and episodes of intense atmospheric and climatic upheaval. During Earth’s geological history, there have been many episodes of global climate change that were of a similar magnitude to the anthropogenically forced climate change that has occurred during the past century. Equally, there are climatic and atmospheric events in the pre-Quaternary past that have been identiﬁed as good analogs of Earth’s climatic future under a doubling of atmospheric

carbon dioxide concentrations ( pCO2) and our aspirational global warming target of no more than 2◦C above preindustrial temperatures. What the paleobotanical record offers in abundance to the study of global change is the dimension of time coupled with a combined set of Earth system boundary conditions, which are more representative of our climate future than any interval during the past approximately 2 million years (the Quaternary period). However, the limitation of using the pre-Quaternary climate record to better understand biological response to global change is also related to time. The temporal resolution available in the geological record of fossil plants is on the order of tens of thousands of years at best, but more often, it is on the order of hundreds of thou- Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org sands to millions of years. Therefore, the paleobotanical record is imperfect, as it offers a window Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. onto individual species, communities, and biome-level responses to global change, in particular to

elevated CO2 and global mean surface terrestrial temperature, yet this view is blinkered by irregu- lar snapshots taken every 10,000 to 100,000 years. This review synthesizes studies in paleobotany that provide important insights into plant and vegetation responses to past global change, from the species to the biome scale, with a particular focus on times in Earth’s history that represent climatic transitions from icehouse to greenhouse states and from mild greenhouse to super-greenhouse states, as it is these intervals that are most representative of Earth’s climate future.

GEOLOGICAL CONTEXT FOR CONTEMPORARY GLOBAL CHANGE The primary drivers of climatic change on a global scale are solar forcing, atmospheric composition, plate tectonics, and the Earth’s biota (25, 56, 129). The relative position of Earth in

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relation to the sun and the age of the sun (51) determines the total solar irradiance at any point in Earth’s geological history. On geological timescales, atmospheric composition is determined by the carbon, oxygen, sulfur, and phosphorous cycles (16, 18), and how they are inﬂuenced by Clathrate: an ice–like Earth system processes. Constituents of the atmosphere that have changed dramatically on ge- solid compound ological timescales include CO2 and O2, both of which force global climate (116, 129). In the composed of methane geological past, intense episodes of global cooling and warming have been linked, respectively, to trapped in the crystal structureofwater the massive release of SO2 from volcanism (158) and CH4 from marine clathrates (70, 91), and thermogenically to volcanic intrusions (59, 152). These gasses, too, have shaped global climate Thermogenesis: and had an impact on Earth’s biota, particularly at faunal mass-extinction boundaries (99, 159), the process by which but on much shorter timescales than CO and O . Both SO and CH are relatively short lived in hydrocarbon gasses, 2 2 2 4 including methane, are the atmosphere; SO2 rains out within years of release and CH4 is highly unstable, soon oxidizing released from kerogens to CO2, but both have left their signatures in the fossil record of plants via isotopic (133) and or organic-rich physiognomic and cellular signatures in leaves (4, 44). However, they are not considered further sediments due to high in this review. Perhaps the most valuable understanding that has come from a deep-time per- temperatures and spective on global climate change is that current Earth system models likely underestimate the pressure Volcanic intrusion: sensitivity of the global mean temperature to atmospheric CO2 (52, 129). Climate sensitivity refers to the change in global mean temperature in response to a doubling of CO over the preindustrial occurs when magma 2 cools before it reaches concentration of 280 ppm (113). Most climate and Earth system models use a climate sensitivity the surface; also called of approximately 3 Kelvin (reviewed in 129); however, analyses of climate sensitivities on longer igneous intrusion geological timescales have concluded that these sensitivities are likely to be underestimated when Physiognomy(ic): considering global temperature and proxy or model CO2 estimates for greenhouse intervals in the the architecture of a geological past (52, 129). This is of considerable concern for policy-makers because knowledge leaf, including shape of the deep-time record argues for much more severe increases in future global temperature than traits of the leaf base, any current climate model predicts under a doubling of CO . According to Foster et al.’s (52, tip and margin, 2 characteristics of p. 1) assessment of greenhouse forcing through time, “If CO2 continues to rise further into the venation, and leaf size twenty-third century, then the associated large increase in radiative forcing, and how the Earth Paleophytic: the time system would respond, would likely be without geological precedent in the last half a billion years.” in geological history when spore-bearing vascular plants VASCULAR PLANTS AND ATMOSPHERE EVOLUTION (pteridophytes) were Broadly, the evolution of vascular plants during the past 420 million years can be subdivided ecologically dominant in the majority of into three distinct evolutionary phases: Paleophytic (old plants), Mesophytic (middle plants), and terrestrial ecosystems; Cenophytic (young plants). The evolutionary phases are temporally offset to those of the evo- often considered from lutionary faunas that deﬁne three stratigraphic eras: Paleozoic, Mesozoic, and Cenozoic, which mid-Silurian to late subdivide the Phanerozoic Eon (155, 166). Plant extinctions at the taxonomic levels of family and Carboniferous

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org order do not coincide with all of the faunal mass-extinction boundaries that characterize the start Mesophytic: the time

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. and end of eras and tend to be more protracted in their nature and more difficult to pinpoint in in geological history geological history (30, 99). Traditionally, the evolutionary floras defined intervals of reproductive when nonangiosperm seed plants dominance (30, 110). (gymnosperms) were Paleophytic ecosystems are typically dominated by vascular spore-bearing plants (pterido- ecologically dominant phytes), including extant lineages such as lycophytes and monilophytes (ferns and Equisetales) in most terrestrial and extinct groups, such as progymnosperms. The Mesophytic era ushered in the dominance of ecosystems; usually seed- over spore-based reproduction for the first time, with gymnosperms typically having greater considered from late Carboniferous to relative abundance in fossil floras than pteridophytes. Extant gymnosperm lineages that had an mid-Cretaceous important role in the Mesophytic era include conifers, cycads, and ginkgos. Finally, the Ceno- phytic era represents a time in Earth’s history when flowering plants (angiosperms) underwent rapid diversification and became dominant within terrestrial ecosystems, ultimately giving rise to the modern flora. It is now recognized that plant evolutionary eras are not only characterized by

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reproductive innovations but also distinguished by unique vegetative and ecophysiological traits (25, 50, 54, 168, 169, 179) that may have changed the competitive landscape in each successive evolutionary era. Cenophytic: the time in geological history The exact geological boundaries of the plant evolutionary eras are quite loose, which is why when angiosperms plants were not used to define the stratigraphic time span of eras, having not been formally defined were ecological or officially recognized by the International Commission on Stratigraphy. For the purpose of this dominant; usually review, the boundary of the Paleophytic and Mesophytic is placed in the late Carboniferous, based considered from on studies that have pushed back the timing of seed-dominated ecosystems, with a distinctly Meso- mid-Cretaceous to present phytic look back to the Carboniferous and Permian (30, 41, 120). In this review, the boundary of the Mesophytic and Cenophytic is not defined by the origin of angiosperms in the earliest Cretaceous Monilophytes: spore-bearing plant (30) but at the time when multiple lines of evidence suggest that angiosperms had attained a global evolutionary group geographical occurrence and many of their reproductively and vegetatively distinctive traits, such comprising all ferns, as increasing floral complexity and high vein densities, are evident, approximately 127–120 Mya horsetails, and whisk (9, 35, 49, 58). Alternatively, the boundary of the Mesophytic and Cenophytic could be placed at ferns approximately 90 Mya, when angiosperms became ecologically dominant in the majority of world Progymnosperms: biomes (89, 166). an extinct group of The Paleophytic era of plant evolution occurred against a backdrop of strongly fluctuating woody spore-bearing plants from which all atmospheric CO2 and global climate at multiple different temporal scales. The earliest vascular seed plants likely arose plants belonging to the Paleophytic era evolved approximately 423 Mya (139) in an atmosphere of Pennsylvanian: strongly elevated CO2 that was more than 10 times higher than preindustrial levels (57, 95, 126), a subperiod of the which then declined by the Carboniferous to levels similar to those of our contemporary icehouse Carboniferous dating world (10, 106), as plant diversity and geographical coverage increased (Figure 1). In turn, the between 323.2 and radiation of land plants resulted in increased carbon sequestration through the chemical weathering 298.9 Mya according of silicates and the burial of organic matter in the great coal swamps of the Carboniferous (3, 106). to the International Commission on New high-resolution, multiproxy records for the late Pennsylvanian document glacial–interglacial Stratigraphy atmospheric [CO2] fluctuations of between approximately 200 and 800 ppm, which coincided with ice sheet contraction and expansion and resultant sea level rise (106). In large part, the Mesophytic

era was characterized by CO2 concentrations above 500 ppm (11, 12, 29, 43, 57, 94, 100, 114, 124, 145, 151, 178) and as high as 2,000 ppm or greater at the boundary of the Triassic and Jurassic periods (23, 135, 143, 177). The Cenophytic era was characterized by a pattern of long-term

decline in CO2 and by global cooling leading to our current icehouse conditions (Figure 2)(7, 52, 57, 63, 65, 68, 82, 93, 119, 122, 132, 140, 144, 149, 160, 162, 180). It has been suggested that the evolution and rise to ecological dominance of ﬂowering plants may have contributed

to the long-term decline in CO2 of the Cenophytic by increasing carbon sequestration through impacts on the long-term carbon cycle (17); however, this hypothesis has not been rigorously

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org tested and, therefore, remains speculative. CO2 was not the only atmospheric constituent gas to

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. change dramatically throughout Earth history; O2 likely also ﬂuctuated wildly, according to some models (16, 19, 61, 105) from lows of <10% to peaks as high as 30%. O2 has an important role in forcing global climate (116) and likely plant evolutionary patterns as well (67, 166, 179). However,

as it will not change considerably during the next two centuries, only CO2 and its impact on plant biology are considered in this review.

THE FOSSIL PLANT RECORD AND PAST GLOBAL CHANGE The Earth’s vegetation has undoubtedly been shaped by climatic and atmospheric evolution during millions of years of geological time. Climate, specifically the mean annual temperature (MAT) and mean annual precipitation (MAP), defines the geographical extent of our modern biomes and plays a fundamental part in defining the ecological niche of species. Often, views of the vegetated Earth

764 McElwain PP69CH28_McElwain ARI 7 April 2018 9:39 Seed plants Spore Spore plants 450 Mya (139); tic, and osperms, > s, ale from the 2013 Gymnosperms Grass Bryophytes Pteridophytes Angiosperms 0 50 Cenophytic 100 150 200 Mesophytic 250 Time (Mya) 300 350 Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. Paleophytic 400 450 Ordovician Silurian Devonian Carboniferous Permian Triassic Jurassic Cretaceous P. Eocene O. Mio. Tropical everwet Tropical summerwet Tropical desertSubtropical temperate Warm temperate Cold Winterwet summerwetSubtropical Grassland sheet Ice 500 pteridophytes, based on the time143.8 of Mya origin (139); of and vascular grasses, plants,Cenophytic), 65 433.5 modified Mya Mya from (148)], (139); Reference biomes gymnosperms, 30. through based Plant time on illustrations (166), the from and time Reference the of 166 timing origin by of of Marlene the seed Hill-Donnelly; phases plants, used of 373.8 with plant Mya; permission. evolutionary angi Geological floras timesc (Paleophytic, Mesophy Figure 1 Time line of plant evolution demonstrating the estimated first occurrences of major plant groups [bryophytes, based on the time of origin of land plant update by the International Commission on Stratigraphy. Abbreviations: Mio., Miocene; O., Oligocene; P., Paleocene.

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a McElwain & Chaloner, 1995; 407 to 400 Mya (1) Haworth et al., 2005; 133 to 104 Mya (9) Doria et al., 2011; 38 Mya (1) Franks et al., 2014; 409 to 13 Mya (15) Du et al, 2016; 121 to 112 Mya (1) Steinthorsdottir et al., 2016a; 36 to 23 Mya (5) Roth & Konrad, 2003; 409 Mya (1) Passalia, 2009; 121 to 101 Mya (16) Roth-Nebelsick et al., 2012; 35 Mya (1) Beerling, 2002; 324 to 270 Mya (24) Mays et al, 2015; 97 Mya (1) Grein et al., 2013; 33 to 17 Mya (4)** Montanez et al. 2016; 312 to 303 Mya (25) Barclay et al., 2010; 94.5 to 93.9 Mya (17) Roth-Nebelsick et al., 2014; 33 Mya (1) McElwain et al., 1999; 202 to 199 Mya (8) Quan et al., 2009; 81 to 72 Mya (9) Erdei et al., 2012; 30 Mya (5) Steinthorsdottir et al., 2011; 202 to 199 Mya (17) Steinthorsdottir et al., 2016b; 67 to 60 Mya (4) Sun et al., 2017; 28.5 Mya (1) Beerling et al., 1998; 205 to 168 Mya (4) Beerling et al., 2002; 66 to 63 Mya (5)* Kürschner et al., 2008; 26 to 12 Mya (18)* Wu et al., 2016; 205 to 171 Mya (3) Royer, 2003; 61 to 54 Mya (2)* Reichgelt et al., 2016; 23 Mya (2) Bonis et al., 2010; 203 Mya (1) Royer et al., 2001b; 60 to 15 Mya (24)* Wang et al, 2015; 13.8 to 1 Mya (7) Chen et al., 2001; 187 to 135 Mya (3) Smith et al., 2010; 50 Mya (3) van der Burgh et al.,1993; 10 to 2 Mya (5)*** Steinthorsdottir & Vajda, 2015; 186 Mya (1) Greenwood et al., 2003; 49.9 Mya (9) Wan et al., 2011; 8.5 Mya (3) Sun et al., 2007; 186 to 139 Mya (7) McElwain, 1998; 47.8 to 44.5 Mya (5) Stults et al., 2011; 8.3 to 3.1 Mya (2) McElwain et al., 2005; 183 to 182 Mya (6) Grein et al., 2011; 47 Mya (1) Kürschner et al., 1996; 4.6 to 2.8 Mya (4) Beerling & Royer, 2002; 168 Mya (1) Kürschner et al., 2001; 44.5 Mya (1) Retallack, 2009a; 233 to 3.9 Mya (17) Yan et al., 2009; 168 Mya (5) Maxbauer et al., 2014; 43 Mya (1) 2,500 RCP 8.5 (2.6 to 4.8°C) RCP 6.0 (1.4 to 3.1°C) RCP 4.5 (1.1 to 2.6°C) RCP 2.6 (0.3 to 1.7°C) 2,000

1,500

1,000

500

Carbon dioxide concentration (ppm) concentration Carbon dioxide 0 450 400 350 300 250 200 150 100 50 0

Time (Mya) 2050 2150 2300 Year b

Neogene Paleogene

Cretaceous Jurassic Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only.

Triassic Permian

(Caption appears on following page)

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Figure 2 (Figure appears on preceding page)

(a) A record of atmospheric carbon dioxide concentration ( pCO2) in parts per million (ppm) during the Phanerozoic based on 47 independent, stomatal-based CO2 proxy studies (7, 10, 12, 14, 23, 29, 34, 42, 43, 46, 52, 57, 63–65, 68, 82, 83, 92–95, 100, 106, 114, 119, 122, 123, 125–128, 132, 135, 140, 143–145, 149–151, 160–162, 177, 178, 180). See Reference 52 for a compilation of raw data from all of these studies, with the exception of 106, which is added here to produce the Lowess regression (heavy blue line) and upper and lower uncertainty bounds. The number in parentheses after each citation refers to the number of pCO2 estimates generated from ∗ each study together with the age range of fossils used to reconstruct CO2. Asterisks indicate use of updated data: single asterisk ( )for data updated by Beerling et al. (2009); double asterisk (∗∗) for data updated by Roth-Nebelsick et al. (2004); and triple asterisk (∗∗∗)for data updated by Kurschner¨ et al. (1996). Blue dots represent mean pCO2 levels from individual studies listed in the ﬁgure. Small green dots represent the minimum and maximum pCO2 estimates from the same studies. The inset graph plots the projected CO2 rise during the next two centuries based on different Representative Concentration Pathways (RCPs) (104) with the anticipated rise in global mean temperature (113). Red boxes highlight the intervals that are a focus of this review. (b) Paleogeographic maps illustrate the occurrence of fossil plant localities (colored dots) possessing evidence for woody fossil taxa (tracheophytes) in time and space derived from the Paleobiology Database (https://paleobiodb.org, CC BY 4.0 International License). Occurrence data were plotted using the Paleobiology Database on June 15, 2017, using the group name tracheophyta. Note the high proportion of exceptionally high-latitude sites with trees through time. Inset graph in panel a has a noncontinuous scale. Abbreviation: Mya, million years ago.

and how it will respond under anthropogenic global change are biased by a contemporary-only view that has insufﬁcient consideration for deep evolutionary history. However, because our climate future will likely be more similar to the Eocene of approximately 50 Mya or stages within the Jurassic or Cretaceous (203 to 65 Mya), it has been argued that we should look back and have greater appreciation for the origin of the modern ﬂora. Many in-depth reviews (25, 30, 99, 139) and books (31, 35, 147, 154) have been dedicated to paleobotany and the evolution of plants. The aim of this section is to provide a brief overview of the past 420 million years of vascular plant evolution that have relevance for, and should be considered in the context of, vegetation responses to contemporary global change. The following six lessons have been gleaned from the deep-time fossil record. 1. All living species, with the exception of those that originated during the past century, natu- rally or through human intervention, have survived an approximately 20-million-year win-

dow of time when the atmospheric CO2 concentration has been at its lowest level (less than approximately 300 ppm)—that is, during the past 304 million years since the Late Pennsylvanian ice age (Figures 1 and 2). Unsurprisingly, this 20-million-year window of

low atmospheric CO2 was accompanied by the lowest mean global temperatures recorded during the past 400 million years (52, 180). Therefore, our contemporary global ﬂora are

adaptedtolowCO2 in relative terms and, remarkably, have survived global cooling and declines in atmospheric CO2 since the Eocene–Oligocene boundary (approximately 34 Mya.) without exceeding normal background levels of extinction (99, 117, 166). This suggests that

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org the vast majority of plant species are resilient and adaptable to climate and atmospheric

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. changes, given sufﬁcient time. 2. Among modern ﬂora are families, genera, and species that have exceptionally long evolutionary histories dating back to the Mesophytic era of plant evolution (Figure 1) when elevated

CO2 and equable global temperatures prevailed (Figure 2). These are predominantly vascular seed plants within the gymnosperms. However, this grouping also includes vascular spore- bearing taxa, which although they may have originated during the icehouse climate of the Carboniferous and early Permian, are lineages that have survived up to the present. All these

lineages experienced nearly 230 million years of Earth’s history when CO2 was considerably elevated above present levels (e.g., >500 ppm). Thus, despite the fact that all of the longest-

lived lineages have survived the past 20 million years of relatively low CO2, they are likely

more adapted to a high CO2 atmosphere, such as that predicted to occur during the next few centuries, than are very recently evolved lineages (such as many angiosperms) that lack the

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genetic memory of super-greenhouse conditions. It is highly likely that many gymnosperms and pteridophytes with the oldest geological origins are preadapted to our climate future (45, 102, 179). These include taxa in which the carbon assimilation rates today (<400 ppm) Representative Concentration are strongly limited by CO2 diffusion from the atmosphere to the site of carboxylation at the Pathway (RCP): chloroplast, due to either low stomatal or mesophyll conductance (102, 108, 109). Both the- four future greenhouse oretical studies (109) and experimental observations (102) project that diffusion-limited taxa gas trajectories will beneﬁt more signiﬁcantly from future increases in CO2 and will have strong increases proposed by the in carbon assimilation rates than those with high stomatal or mesophyll conductance. Intergovernmental Panel on Climate 3. The grass family, Poaceae, to which all grass-based food crops (such as wheat, barley, and Change rice) belong, originated relatively recently, approximately 65 Mya during the Late Creta- Paleocene–Eocene ceous (148). Grass-dominated biomes—such as steppes, prairies, and savannahs—have an thermal maximum exceptionally recent origin in the context of land plant evolution, expanding globally in the (PETM): the timing majority of continents during the Late Eocene to Oligocene (<35 Mya) (148), concurrently of a rapid global with falling CO2 levels (Figure 2 and references therein), declining global temperature, and temperature warming increasing continental aridity. Therefore, in relative terms and in the context of long-term at the boundary of the Paleocene and Eocene climatic and atmospheric history, the evolutionary success of grasses occurred under the epochs around declining atmospheric CO2 that led to our current icehouse. Prior to the origin of grass- 55.5 Mya dominated ecosystems, savannahs of pteridophytes (ferns and Equisetales) prevailed where climate conditions did not support fully wooded vegetation. 4. It is clear from a wealth of paleobotanical studies (69, 97, 120, 121, 148, 166) that pa- leobiomes have waxed and waned in lockstep with global climate over geological time (Figure 1). A few observations from these studies stand out. First, during times of high

atmospheric CO2 concentrations and global warmth, the temperature gradient between the equator and pole is shallow (Figure 3), which results in fewer (<5) distinct vegetation biomes compared with today’s 10 biomes in an icehouse climate (Figure 1). Second, based on current understanding of atmospheric composition using stomatal proxy records, it appears that a tropical rainforest biome was absent from the low latitudes when atmospheric

CO2 was higher than approximately 700 ppm (Figures 1 and 2, and references therein). According to the future carbon use projections in Representative Concentration Pathway

(RCP) 6, CO2 will reach 700 ppm by 2150, and RCP 8.5 projects that this level will be reached well within this century (Figure 2) (113). Further paleobotanical studies are ur-

gently required to establish whether such an apparent CO2 threshold for the existence of a tropical everwet biome (tropical rainforest) is robust or whether its absence for much of the Mesophytic was due to the fact that the traits that are used to deﬁne our understanding of a modern tropical rainforest, such as high leaf-vein density (25), had not yet evolved in the

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org gymnosperm-dominated taxa of the Mesophytic. Alternatively, there is also a chance that

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. a tropical rainforest biome was present in the Mesophytic but remains undetected because of an absence of fossils, localities, or both in the low tropical latitudes (Figure 2)orbe- cause existing fossil plant assemblages have been wrongly classiﬁed in terms of their biome characterization. Palynological (or palynomorph, meaning pollen and spore) studies of low-latitude tropical rainforests with modern characteristics have shown that they date back to the Paleo- cene (75, 78, 174). It appears that these forests survived the extreme global warming event of approximately 5 to 8◦C MAT during more than 200,000 years at the Paleocene– Eocene thermal maximum (PETM) (103) 56 Mya, with little evidence of extinction, but instead showed a strong signal of resilience. In the tropics of Colombia and western Venezuela, a palynological study suggested that tropical rainforest vegetation increased diversity in response to global warming at the PETM (76). This ﬁnding strongly contradicts

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ac 40

Eocene 20 Fossil forest 1

Modern

MAT (°C) –20

–40

–60 Fossil forest 1 profile 90°N 60°N 30°N 0 30°S 60°S 90°S Latitude 40 m b 40

35 Fossil forest 2 30 25 m 25

20 Fossil forest 2 profile MAT (°C) 15

0 90°N 60°N 30°N 0 30°S 60°S 90°S Latitude Land surface MAT (modeled) Land surface MAT (from proxies) Tropical sea surface temperatures (from proxies) Tropical sea surface temperatures (modeled)

Figure 3 (a) Comparison of modern (blue dashed line) versus Eocene (red solid line) model of the mean annual temperature (MAT) profile from Huber & Caballero (73), demonstrating the marked polar amplification of MAT under an extreme Eocene CO2 greenhouse forcing of >4,000 ppm. Eocene MAT records according to latitude are based on paleo MAT proxy data compiled by Huber & Caballero (73). Forcing the model with >4,000 ppm is currently the only mechanism for achieving a good match between data and model, suggesting Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org that the climate sensitivity of current Earth system models is not sufficiently sensitive to CO2 (52) or that other greenhouse forcing

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. variables that are not included, such as methane or water vapor, had important roles in equable Eocene climates. (b) There is generally good agreement between proxy data and model estimates of MAT when a high CO2 forcing of 4,000 ppm is used. (c)The ◦ reconstruction of a high-latitude (75 to 80 N) Eocene-aged Metasequoia glyptostroboides forest is based on fossil tree stumps found in situ on Axel Heiberg Island, Canada, from Reference 165. Fossil forests at two nearby sites were discovered, including a slightly older forest (fossil forest 1) and a slightly younger forest (fossil forest 2). Adapted with permission from References 165 and 73.

future-model projections of ecosystem collapse in the tropics (33). The record of atmo-

spheric CO2 change associated with this warming event remains unconstrained, however, so it cannot yet be determined whether 700 ppm (Figure 1)isaCO2 threshold for tropical rainforest survivability. 5. The tundra biome was absent for much of Earth’s vegetated history (Figure 1). This startling observation will be elaborated on in further detail in the section Polar Ampliﬁcation and Past Vegetation Responses.

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6. Finally, the current differentiation of biomes into 10 distinctive vegetation units is a distinctly modern phenomenon that likely had its origin in the Miocene, only 11 Mya (Figure 1) (166).

POLAR AMPLIFICATION AND PAST VEGETATION RESPONSES Greenhouse gas–induced global change will not result in equivalent warming levels in all parts of the world. Due to a phenomenon referred to as polar amplification, the Earth’s poles have warmed (72) and will continue to warm at a faster rate and reach a higher magnitude of relative warming than the average planetary warming (138). This is because heat is readily transported poleward by oceans and the atmosphere due to positive feedback effects involving snow cover, albedo, vegetation, soot, and algal cover in the Arctic and Antarctic, and to many other Earth system phenomena that appear to amplify polar warming as the greenhouse gas concentration in the atmosphere rises (for a detailed review, see 138). The question is, Will global change have a disproportionate impact on plant biology, ecosystem function, ecology, and feedback in the highest latitudes of our planet due to the phenomenon of polar amplification? Recent, historical satellite data sets document the greening of the tundra biome (79), the range expansion of woody shrub (107) and tree taxa (reviewed in 28) into tundra systems, and a general increase in woody plant biomass and relative abundance (107). Considerable scientific effort is focusing on how such vegetation changes will feed back to the Arctic climate system via changes in carbon sequestration and the water cycle and changes to surface irradiance (reviewed in 107). Increasing shrubiness has likely already had an unexpected negative impact on herbivore populations, such as caribou, by decreasing browse quality (48). Furthermore, field-based evidence for woody plant responses to amplified Arctic warming is not all positive. Reduced tree growth has been observed for some taxa due to drought-induced stress (6) and negative biotic interaction, such as bark beetle infestation. Satellite normalized difference vegetation index data have recorded areas of browning that indicate productivity loss as well as greening in Arctic vegetation (79). Furthermore, a large percentage of Arctic vegetation among all plant functional types has shown no perceptible change in productivity in response to contemporary global change (79). Owing to the fact that shifts in ecological composition, the ecophysiological function of vegetation, or both can have a large impact on the climate and on the biotic system as a whole, it is important to predict whether short-term temporal trends in Arctic vegetation change will continue under

CO2-induced global warming. The paleobotanical record of high Arctic ﬂoras may provide broad insight into these questions. The geological record is replete with high polar fossil ﬂoras demonstrating fully wooded ecosystems at paleolatitudes as high as 79◦N (62, 142, 163, 165) and 75◦S (36, 47, 53, 80, 115, 118),

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org ranging in age from 290 Mya in the Permian Antarctic (153) to approximately 23 Mya (early

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. Miocene) in the Arctic (71) and to approximately 37 Mya in the Antarctic (late Eocene) (Figure 2) (156). Collectively, these polar fossil forests demonstrate that fully wooded terrestrial ecosystems with tree densities similar to modern forests, occurring today at temperate and tropical latitudes

(115, 165), can be sustained in the high Arctic and Antarctic when the global atmospheric CO2 concentration is >500 ppm (Figure 2 and references therein) and greenhouse-induced forcing of 5W/m2 is evident (52). The presence of high-latitude forests in the geological past also highlights the extreme vulnerability of the contemporary tundra biome, which is notable for its apparent absence for millions of years of Earth history during times of high global warmth and elevated

CO2 concentrations (Figures 1 and 2). Based on biome reconstructions (Figure 1) (166) and the documented presence of polar forests (Figure 2), it appears that the tundra biome as deﬁned today did not exist for the majority of the Mesophytic era of vascular plant evolution and the early

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Cenophytic up to the time of the inception of Antarctic ice sheets at around the Eocene–Oligocene boundary, approximately 34 Mya (180). Paleobotanical studies have demonstrated that during the early Eocene (56 to 49 Mya), a time of peak sustained global warmth during the past 65 million years (Figure 3) (73), the Arctic Ocean was ice free (Figure 1) and fringed by a mosaic of mixed deciduous (Carya, Liquidambar, Ulmus, Larix), evergreen (Picea, Pinus), and swamp (Metasequoia, Glyptostrobus) forests (62), and teeming with high densities of the aquatic fern Azolla (8). Estimated canopy heights of between 25 and 40 m have been reconstructed for Metasequoia forests at 79◦N, with aboveground paleoproductivity estimates ranging from 2.8 to 5.5 Mg/(ha·year) (Figure 3), which is thought to be similar to that observed today in old growth temperate rain forests in the north Pacific (165). The presence of Azolla is attributed to high levels of runoff into the Arctic Ocean resulting in a sufficient freshening of the seawater or the development of a freshwater cap suitable for its survival and proliferation (27, 32). Substantially higher precipitation in the Arctic than modern levels is also supported by isotopic analyses of fossil tree rings (136) and leaf physiognomy studies (163), although the definition of the seasonal pattern of rainfall remains disputed—that is, whether it was predominantly summerwet (136) or year round (163). The eventual demise of Azolla in the Arctic Ocean is attributed to reduced runoff and a slight salinity increase (8). The presence of a freshwater fern in the Eocene Arctic Ocean is a remarkable demonstration of the possible consequences of global change in Arctic terrestrial ecosystems and of threshold behavior linking terrestrial and ocean systems via runoff (27). Numerous Earth system models

predict increased global runoff under future elevated concentrations of CO2 as a direct response to reduced transpiration of global vegetation (60). Although the Eocene Azolla studies have not considered that physiological forcing of the climate by Arctic vegetation affected fluctuations in runoff and, instead, attributed changes to altered precipitation patterns and amount alone, such a study is warranted and possible through the examination of fossil cuticle archives in Arctic fossil floras. Such studies are discussed later in this review, with a case example from the late Triassic mass-extinction event (approximately 200 Mya). An interesting side note is that Azolla is now considered a potential candidate taxa for negative carbon emission measures because of its phenomenal growth rate and carbon sequestration potential. Based on overwhelming paleobotanical evidence, it is highly likely that the current northward migration of woody tree and shrub taxa into the Arctic, along with the general greening (reviewed in 28, 107), will continue and, in doing so, will drive positive feedback of the climate system that will further accelerate the warming and wetting of the Arctic (74, 163). In the past, high polar forests had carbon sequestration potentials (13, 115, 131, 165) equivalent to those of the much lower temperate latitudes, and they impacted the hydrological cycle sufficiently to alter ecological

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org dominance patterns within oceans (8, 27). These ﬁndings from paleobotanical studies suggest that

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. the role of Arctic vegetation in the global biogeochemical cycling of water and carbon will become increasingly important if we continue on a path of intense petroleum use.

PAST GLOBAL CHANGE AND IMPACTS ON PLANT COMMUNITY COMPOSITION Future global change is predicted to alter the ecological composition of plant communities because species are highly individualistic in their responses to climate change. Species differences in migration rate, invasive capacity, resilience in the face of climate change, and extinction tolerance will all result in the emergence of plant communities that have no past or modern analogs and that occupy climate envelopes or niches that may not have a historical or modern precedent. What will these future communities look like? This complex question can be addressed using different

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approaches that include, but are not limited to, climate niche modelling and in-situ ﬁeld-based

experiments with elevated CO2 concentrations, such as free-air CO2 enrichment (FACE) studies, demographic modeling, examination of plant trait relationships along spatial gradients of MAT Free-air CO2 enrichment (FACE): and MAP, and comparative ecophysiological modeling and experimentation. Rarely are insights in situ open-air from the pre-Quaternary paleobotanical record incorporated or discussed in the context of these elevated CO2 different methodologies. In the next section, I briefly review some of the key findings from these experiments where studies of contemporary vegetation and examine predictions of future plant community–level re- mature established sponses to global change in the context of the paleocommunity responses to past global change. native vegetation or crops are exposed to Does the fossil plant record support or refute some of the landmark findings and predictions of elevated CO2 modern ecological and ecophysiological studies? treatments over long durations and compared with Extinction, Migration, and Past Global Change ambient CO2 controls The deep-time fossil record paints a picture of remarkable resilience in the face of extreme climate change that surpasses in magnitude both contemporary and future predicted mean global terrestrial temperature rises (76, 99, 166, 170). However, one important distinction is that the rate of anthropogenic climate change far exceeds that of any well-characterized greenhouse-induced global warming event in the deep geological past. Plant family- and generic-level extinctions are rare in the fossil record even at the big five mass extinction boundaries, which recalibrated the evolutionary clock of the animal kingdom with family-level extinctions of more than 50% (166). Some of the best-studied intervals of global change in the fossil plant record include the Triassic– Jurassic boundary, 201.36 ± 0.17 Mya (175); the PETM, 56 Mya; and the Eocene–Oligocene boundary, 33.9 Mya. The first two events represent rapid greenhouse gas–induced global warming episodes; the last coincides with the initiation of the Antarctic ice sheet and global cooling leading to our current icehouse. Therefore, I focus on the first two events and the common patterns that have emerged from studying them, despite the fact that they are separated by millions of years of plant evolution and, thus, are characterized by vastly different phylogenetic landscapes from each other and from the modern world. Analyses of the Triassic–Jurassic boundary and the PETM have documented clear evidence of local extinction, but not global extinction, and both intra- and intercontinental-scale migration resulting in dramatically altered plant community composition and dominance patterns (76, 90, 98, 103). During the PETM, compositional shifts in terrestrial vegetation were marked but transient in temperate latitudes (103) and long-lived in the tropics (76). High temperatures and likely increased aridity in the North American temperate biomes resulted in geologically rapid compositional changes as local mixed deciduous and evergreen forest taxa—such as Betula, Lau-

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org rus, Ulmus, Cercidiphyllum, Carya,andTaxodium—decreased in relative abundance, and southern

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. subtropical Leguminosae expanded their range northward by up to 1,000 km (103). A somewhat surprising finding in the tropics was an increase in standing diversity as global temperatures rose by 5◦C within 10,000 to 20,000 years but tropical precipitation remained at least stable, resulting in only muted levels of extinction and a large increase in originations (103). However, despite low extinction rates, significant compositional shifts are evident in the tropical pollen and spore records at the PETM (76) and during the End-Triassic (90). These paleo examples strongly suggest that global warming has a marked effect on the composition of terrestrial plant communities that is driven predominantly by migration rather than extinction. Admittedly, it is difficult to draw parallels with Anthropocene warming and vegetation responses because they are occurring at a minimum of 20 times faster than any past warming episode in Earth’s history (reviewed in 40). A rough comparison of climate velocities (the distance per unit of time that a species needs to migrate to keep within its existing climate envelope) for the PETM (0.05 to 0.1 km/year, based on

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172) and that predicted for the end of this century under an RCP 8.5 scenario [0.5 to 128 km/year (40, 88)] identiﬁes a stark mismatch between what the fossil record demonstrates is possible and what future predictions indicate will be necessary for taxa to remain within their climate niches.

Closer examination of an alternative future scenario with less elevated CO2 concentrations (and climate velocities of 0.01 to 12 km/year) (40, 88) provides some hope, however, as PETM climate velocities at least map onto the lower range of future predictions.

Paleobotany, Adaptation, and Past Global Change Plants have alternative strategies for surviving global change beyond migrating and maintaining their existing climate envelope, including acclimation and adaptation. However, investigating the adaptive capacity of individual species is complex because it requires observations of multiple generations and, therefore, requires experiments of long duration, which are rarely feasible. Al- ternatively, space-for-time studies are often employed using the spatial gradients in MAT, MAP, or both as surrogates for climate change; however, these studies are limited because they cannot

account for the impact of anthropogenic CO2 rise. Paleobotanical studies offer a means of exam- ining plants’ capacity to adapt to global change on timescales of tens of thousands to millions of years and, perhaps more importantly, help to define the limits of species’ environmental tolerance in the geological past. An important set of prerequisites for such fossil-based studies is that (a)the magnitude and pace of paleoenvironmental change is well characterized from plant-based proxies and independently verified with nonplant-based proxy approaches so that circularity is avoided, and (b) multiple fossil plant beds are preserved in the same geological sections, thus offering regular snapshots of plant community composition, paleophysiology, and diversity from before, during, and after the global change interval. Such fossil localities provide rare study systems where species-, generic-, and community-level attributes that provide measures of ecosystem stability and resilience can be tracked in response to past global change. They can also be examined to elucidate traits that increase extinction risk and those likely to confer resilience in the face of global change, both of which may have relevance for current conservation efforts. One study system that has yielded a wealth of data relevant to contemporary issues of climate change and vegetation responses occurs at a field locality called Astartekløft in East Greenland. This fossil plant locality preserves sediments and fossil plant beds within the Kap Stewart Group that span the End-Triassic mass extinction event (ETE) and the ensuing recovery interval that occurred in the Earliest Jurassic (Figure 2).

The End-Triassic Mass Extinction Event Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. The ETE, dated at 201.56 Mya (175), was the third greatest faunal mass extinction event in Earth’s

history (137). It is characterized by an episode of intense CO2-induced global warming (98) that was triggered by both intrusive and extrusive volcanism (reviewed in 38) associated with the Central

Atlantic Magmatic Province. Atmospheric CO2 and global temperature changes associated with the ETE are well characterized from multiple proxy sources, and they document a geologically

rapid trebling of CO2 concentrations from pre-excursion levels of approximately 600 ppm to levels >2,000 ppm (Figures 2 and 4) (23, 94, 135, 143, 177). These paleo CO2 estimates were made using the stomatal-based proxy method applied to Triassic and Jurassic fossil cuticles from Greenland (94, 143), Sweden (94), Germany (23), Northern Ireland (143), and China (177), and they were independently veriﬁed from fossil soil–based proxies (135). The End-Triassic global change event

occurred at a substantially slower pace than contemporary anthropogenic CO2 increases, and it was initiated at a time when the pre-excursion atmospheric CO2 concentration was higher than

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Triassic Jurassic

4,000 a PeakPeak extinctionextinction andand globalglobal warmthwarmth

3,000

(ppm) 2,000 2 CO p 1,000

0 5 b 4

(DCA 1) 2

1 Ecological composition

0 (number of fossil plant genera) 70 c Generic diversity 60 40

50 30 Immigration from lower latitudes 40 20 Paleolatitude signal (°N) 30

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Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. Height in cliff section (cm)

Figure 4 Compilation of global change and biological responses recorded at Astartekløft, East Greenland, associated with the End-Triassic extinction event. (a)CO2 change ( pCO2) (143). CO2 estimates based on calibrations using a transfer function of Barclay & Wing (2016) ( gray triangles) and the Carboniferous standardization ( gray diamonds) and recent standardization ( gray squares) of McElwain (1998). (b) Plant compositional response as indicated by detrended correspondence analysis (DCA) axis 1 scores from relative abundance data (98) ( green diamonds). Note that the numerical scale plots fossil plant communities (assemblages), which are compositionally similar in terms of their relative abundance distributions, closely together and those that are compositionally distinct further apart. (c) Plant migration responses in relation to paleolatitude (◦N) (98) (brown diamonds) and plant generic diversity trends (blue squares) based on relative abundance distributions of fossil plant taxa (101). The x-axis refers to the height of the geological cliff section from which fossil plants were sampled, with time going from older to younger with height. Landscape visualizations by Marlene Hill-Donnelly; used with permission. Abbreviation: ppm, parts per million.

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today (approximately 600 ppm). However, the total estimated magnitude of CO2 increase that prevailing plants were exposed to (e.g., an addition of approximately, 1,740 ppm) is similar to that expected by the year 2250 under RCP 8.5 (e.g., an addition of approximately 1,660 ppm between Bennettitales: an preindustrial years and the year 2100) (Figure 4). If more conservative estimates of Late Triassic extinct group of seed CO2 rise are considered (e.g., an addition of 990 ppm to the Late Triassic atmosphere), an equiv- plants with unisexual alent magnitude of CO2 rise will occur well before 2150 under an RCP 8.5 scenario (Figure 4). or bisexual ﬂower-like Therefore, the Late Triassic global warming event occurred at a considerably slower pace (12 reproductive times slower than RCP 2.6 and a whopping 280 times slower than RCP 8.5) than modern global structures; diverse and geographically warming, but the event had a greater overall magnitude than contemporary anthropogenic forc- widespread from the ing. Although it is an imperfect analog, it highlights the acuteness of current global change and Early Triassic to Early provides a window through which to study the adaptive capacity of plant traits, species, and whole Cretaceous communities in the past. Pangea: a supercontinent made up of Eurasia, Africa, Case Study of Past Global Change: Astartekløft, East Greenland North and South America, Australia, Paleobotanical studies indicate that forested, gymnosperm-dominated ecosystems at Astartekløft, Antarctica, and India East Greenland, underwent rapid compositional shifts during the Late Triassic as atmospheric that existed between CO2 reached 1,000 ppm (94), which was followed by 85% species-level turnover coincident with approximately 355 and 170 Mya afurtherCO2 rise to 1,500 ppm (94, 143). Although only one plant family suffered global extinction, extirpation was marked at the species level (98, 158, 159), on the basis of detailed study of macrofossils (mainly fossil leaves), and at the generic level (112), on the basis of detailed study of palynomorphs (fossil pollen and spores).The extinction of reproductive specialists ranged from regional extinction (Bennettitales) to global extinction (Lepidopteris), whereas wind-pollinated gen- eralists proliferated in the aftermath of the species turnover event (ferns and fern allies, Ginkgoales) in East Greenland and Southern Sweden (90, 98). In other regions of the supercontinent Pangea and in East Greenland, the ETE is marked by a geologically transient ecological dominance of ferns and fern allies (87) belonging to extant fern families, many of which today have exclusively tropical and subtropical biogeographical distributions. Thermophilic conifers belonging to the extinct Cheirolepidiaceae family became dominant in the continental interiors in many global localities (22), perhaps aided by widespread ﬁre disturbance (15) and their likely capacity for whole-genome duplication (81), which is generally rare in gymnosperms.

Therefore, the pattern of global vegetation responses under super-elevated CO2 is characterized by a loss of evenness (101) and local-to-regional–scale turnover (22, 87, 90, 98), but remarkably little global extinction at higher taxonomic ranks (30, 166). Competition was the predominant fac-

tor shaping the assembly of communities under progressively rising CO2 concentrations, and the

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org ecological dominance of some taxa increased sharply (101). Rare taxa appeared to be preferentially

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. lost from the Late Triassic ecosystems of East Greenland as a result of rising CO2 (101). This deep-time case study supports many of the predictions of ecological theory about how communities respond to environmental stress but do so on evolutionary timescales. The studies also highlight the idea that catastrophic predictions of a dead zone future Earth are likely unfounded but that dramatic ecological shifts should be expected. Modern global change is occurring at a much faster pace than that characterizing the ETE; however, there is strong evidence for widespread transient

migration to higher latitudes in the Northern Hemisphere that coincided with the zenith of CO2 rise and global warming (90, 98), similar to the pattern seen at the PETM in North America (103, 171, 173). A rough calculation based on the macroﬂoras in East Greenland documented the occurrence of species usually found at paleolatitudes of 45◦N occurring >2,000 km northward in fossil localities higher than 65◦N during the peak global temperature excursion, which coincides with fossil plant bed 6 at Astartekløft (Figure 4) (98). This migration rate (approximately 0.01 to

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0.02 km/year) represents a climate velocity at the very lowest estimated rates required by modern

floras to keep pace with anthropogenic climate change under an A1B future CO2 scenario (88). Despite evidence for a strong pattern of northward migration in the Northern Hemisphere, Climate velocity: the estimated rate at which immigrants accounted for only a small percentage of early Jurassic floras, and within approximately a species must migrate 200,000 years, stable forested ecosystems had been reestablished and were predominantly made along the Earth’s up of species that were already present in the forest communities of the latest Triassic (90, 98). surface to maintain a Therefore, the major ecological pattern to emerge from both fossil leaf and palynomorph studies constant mean annual of Astartekløft is generic-level resilience to extreme global warming with lower environmental and temperature under global climate change ecological tolerances at the species level. Furthermore, although migration is evident, suggesting that species moved to maintain their climate envelope as global and regional temperatures warmed, Maximum stomatal there is also strong indirect evidence for in situ adaptation in leaf functional traits (4, 5, 15, 94, 141, conductance ( gmax): calculated as a function 146) and speciation (66, 98) on 100,000-year timescales in response to the ETE global warming of stomatal density and event. This is a facet of vegetation response to climate change that is not well accounted for in pore size; measures the climate niche, physiological, or dynamic vegetation models because the prevailing paradigm based maximum rate at on Quaternary palynological studies assumes climate niche conservatism (164). which CO2 can diffuse into a leaf and water can diffuse out TRAIT ADAPTATION AND PHYSIOLOGICAL FEEDBACK DNA is not preserved in the deep-time fossil record (166). So how can pre-Quaternary-aged fossil plants or parts of them be used to investigate the capacity of a species to adapt to global change? This is particularly complicated by the paleobotanical species concept, which is based on morphological or anatomical traits, or both, which may not be plastic. For example, two fossil plant species defined using aspects of their leaf morphology may represent ecotypes providing evidence for adaptation in response to global change or two separate species in which the speciation event is completely unrelated to the prevailing global change. Trait-based paleobotanical studies offer one method of addressing this limitation. Paleoecological studies of important traits relating to the leaf economics spectrum (176) demon-

strate the adaptation of leaf mass per area (LMA) in response to CO2-induced global warming associated with the ETE (141), PETM (37), and the Cretaceous–Tertiary (21) mass extinction event. Soh et al.’s (141) study showed that global warming selected for fossil plant taxa with high LMA following the ETE, thus providing the ﬁrst evidence on evolutionary timescales that high

CO2 selects for an ecological stress tolerance strategy. The widespread dominance of evergreen taxa during the Eocene (157), which likely had high LMA, provides further support for this pattern. Soh et al.’s study (141) determined that high plasticity in leaf economics traits, such as LMA, was a clear advantage for the longevity of the genus Ginkgo, a living-fossil taxon that has survived

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org to the present.

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. Other examples of important ecophysiological traits that have been tracked in response to past global change include water-use efﬁciency (11, 39, 54, 168), maximum stomatal conductance

( gmax) (55, 84, 102, 169), and xylem conductive capacity (24, 167). Although studies of these types of traits are in their infancy, results suggest that plants have adapted to past elevated CO2-induced global change by decreasing stomatal conductance (54) and increasing their water-use efﬁciency, which on geological timescales has had a positive feedback effect on the regional hydrological cycle by increasing runoff (146, 168) and on the carbon cycle by changing the sink strength of the terrestrial biosphere (106). Differences in the magnitude of the water-use efﬁciency response

to CO2 among fossil taxa have also signiﬁcantly impacted the competitive landscape at critical climatic thresholds, such as the transitions from interglacial to glacial in the Late Pennsylvanian

(168) and elevated to super-elevated CO2 climate states during the ETE (146).

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Predictions from general circulation models (GCM) that have proposed dramatic increases

in future global runoff in response to a doubling of CO2 (20, 60) have been strongly criticized based on results from FACE studies at mature temperate forest sites (86, 134). Schafer¨ et al.

(134) argued that forest feedback on the hydrological cycle under elevated CO2 concentrations would be highly dependent on species composition because the directionality and magnitude of

canopy transpiration responses to elevated CO2 following 3.5 years of exposure were found to be species speciﬁc. Leuzinger & Korner¨ (86) suggested that the physiological effect of elevated CO2 concentrations on transpiration was much lower than expected from theory and from leaf-level

observations of stomatal conductance responses to CO2. They argue that the seasonal pattern of precipitation was a much more important predictor or determinant of ﬂood risk than physiological forcing of the hydrological cycle via reduced transpiration in temperate forests. However, when the potential physiological forcing of climate and the hydrological cycle are viewed through the lens of paleobotany, the global predictions of enhanced runoff using GCMs are by no means extreme. A change in river architecture in the Jameson Land basin in East Greenland—from slow-moving and meandering in the Late Triassic to fast, erosive braided systems in the earliest Jurassic—was likely driven by an estimated 50% reduction in canopy-level transpiration

under intense CO2-induced global warming (146). Geological evidence of increased runoff associated with the ETE includes changes in stream current directions and transient oceanic anoxia in marine sediments (146). Furthermore, within-genus reductions in leaf-level stomatal conductance were accompanied by ecosystem-level shifts in community composition that resulted in community-weighted reduction in overall canopy transpiration. Speciﬁcally, Late Triassic forests dominated by Bennettitales with high leaf-level transpiration rates (146) and low LMA (141) were replaced by dominants from within the Ginkgoales family that had higher LMA and lower leaf-

level transpiration. This is an example in which exposure to CO2 over hundreds of thousands of years resulted in both species-level adaptation (a reduction in stomatal density and pore size

and hence gmax) and community-level compositional changes (98), which altered the function of the vegetation as a whole toward more conservative water use, less recycling of water through the vegetation, and, hence, enhanced runoff. These observations on more than 100,000-year timescales support predictions from general circulation models of increased runoff due to a re-

duction in canopy-level transpiration resulting from elevated CO2 concentrations (60), and they are contrary to ﬁndings from some FACE studies that have been too short to account for community composition changes as well as leaf-level adaptation of functional and economic traits (86, 134).

PALEOBOTANICAL INSIGHTS ON CO2 FERTILIZATION Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. OF PHOTOSYNTHESIS FACE studies on crops and both maturing temperate forests and those that have achieved

full canopy closure have shown a strong and sustained CO2 fertilization effect on net primary production (2, 85, 111) due to an increase in leaf-level photosynthetic carbon gain (1), despite

downregulation of RuBisCO activity (85). However, the typical elevation of CO2 of >200 ppm above ambient concentrations in FACE studies is subtle when considered in the context of future

projections, such as RCPs 6.5 and 8.5. Will CO2 fertilization be maintained in an ambient atmosphere of ≥500 ppm, or is it more likely that photosynthetic carbon gain will saturate? This is an important question with regard to budgeting the future carbon sequestration potential of forests

and vegetation as a whole in a high CO2 world. CO2 has been >500 ppm for the majority of the past 500 million years. Theoretically, therefore, species with RuBisCO-limited photosynthesis and high

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resistance to CO2 diffusion (102, 109) likely had much higher leaf-level saturation of photosyn-

thetic rates for much of the past than their ancestors do today in a comparatively CO2-starved world. There is no clear consensus on the deep-time evolution of photosynthesis in vascular plants from studies using proxy estimates from fossil leaves (26, 96, 102) or model estimates derived from fossil leaf traits (54). Similarly, there remains a wide range of opinions on the evolution of the productivity of terrestrial ecosystems through time and whether modern systems are the most productive (24, 25) or less so than those of the geological past (such as the Eocene), assuming a positive correlation between diversity and productivity (77, 130). What is clear, however, is that the total area of forested ecosystems expands dramatically poleward during greenhouse intervals (Figures 1 and 2), which on evolutionary timescales enabled a greater speciation rate during the Cenophytic era and likely higher productivity in many biomes because of a species-area effect (77). Therefore, the fossil record of Mesophytic and Cenophytic paleobiome distribution suggests that the carbon sequestration potential may increase under moderate greenhouse climates of

between 500 and 700 ppm CO2 (Figure 1). However, a detailed carbon stock assessment of the Paleophytic era has highlighted the switching of carbon sequestration potential between the glacial and interglacial climate, with glacials surprisingly sequestering more carbon in the tropics

than during the interglacials (106). Thus, the jury remains out on the CO2 fertilization effect at concentrations >500 ppm. It is essential and possible, now that the boundary atmospheric conditions are better constrained than ever (Figure 2), to undertake a quantitative inventory of the carbon sequestration potential of the terrestrial biosphere through geological time using a combination of paleo leaf economics traits and dynamic vegetation modeling to address this critical question further.

SUMMARY POINTS 1. The majority of extant plant species, with the exception of those that originated during the Anthropocene, have survived a period of approximately 20 million years when the

atmospheric CO2 concentration was exceptionally low (<300 ppm) as viewed in the context of atmospheric composition during the past 400 million years of Earth’s history. 2. Paleobotanical studies of the tropical rainforest biome suggest that it is much more resilient to global change than predicted by Earth system models. 3. The widespread occurrence of fully forested ecosystems at high polar latitudes in the ge-

ological past during conditions of elevated CO2 concentrations conﬁrms that the tundra

Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org biome is the biome most threatened by future global changes. Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. 4. Paleoclimate data and the presence of polar forests support the concept of the polar

ampliﬁcation of climate during elevated CO2 concentrations. 5. Evidence for enhanced runoff into the Arctic during episodes of past global warmth, such as the Eocene, support suggestions that high Arctic vegetation will have a much more important role in the biogeochemical cycling of carbon and water toward the end of this century if we continue on a path of proﬂigate fossil fuel use and changes in land use. 6. The estimated climate velocities for plant migration associated with the PETM and ETE global warming events were much slower than those that are believed to be required for extant taxa to keep pace with future climate change based on future worst-case carbon-use scenarios, such as RCP 8.5.

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7. The pace of Anthropocene climate change is without geological precedent, yet past global change events of much greater overall magnitude are evident in the fossil plant record. 8. Catastrophic predictions of a future dead zone planet Earth and direct climate-driven extinctions are unfounded based on evidence from the plant fossil record; however, dramatic ecological shifts in dominance patterns should be expected. 9. Trends in paleoproductivity based on evidence from the plant fossil record and the evolution of photosynthesis remain hotly debated and are important areas for future research. 10. Overall, the Earth’s vegetation is much more resilient to global change than many contemporary-only studies would predict because the fossil record demonstrates that many taxa are preadapted to our climate future and others can adapt in situ, and many that have unchangeable climatic envelopes likely have climate velocities that are just about sufﬁcient to keep pace with future global change as long as we take a more sustainable path of future carbon use.

DISCLOSURE STATEMENT The author is not aware of any afﬁliations, memberships, funding, or ﬁnancial holdings that might be perceived as affecting the objectivity of this review.

ACKNOWLEDGMENTS Shanan E. Peters is thanked for generating the fossil plant occurrence maps through time for Figure 2 from The Paleobiology Database (https://paleobiodb.org/#/). Funding from Science Foundation Ireland is gratefully acknowledged (grant number 11/PI/1103). Joseph White and Isabel Montanez˜ are thanked for discussions on the subject of this invited review.

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Annual Review of Plant Biology

Volume 69, 2018 Contents

My Secret Life Mary-Dell Chilton ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp1 Diversity of Chlorophototrophic Bacteria Revealed in the Omics Era Vera Thiel, Marcus Tank, and Donald A. Bryant pppppppppppppppppppppppppppppppppppppppppp21 Genomics-Informed Insights into Endosymbiotic Organelle Evolution in Photosynthetic Eukaryotes Eva C.M. Nowack and Andreas P.M. Weber ppppppppppppppppppppppppppppppppppppppppppppppp51 Nitrate Transport, Signaling, and Use Efﬁciency Ya-Yun Wang, Yu-Hsuan Cheng, Kuo-En Chen, and Yi-Fang Tsay ppppppppppppppppppppp85 Plant Vacuoles Tomoo Shimada, Junpei Takagi, Takuji Ichino, Makoto Shirakawa, and Ikuko Hara-Nishimura ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp123 Protein Quality Control in the Endoplasmic Reticulum of Plants Richard Strasser ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp147 Autophagy: The Master of Bulk and Selective Recycling Richard S. Marshall and Richard D. Vierstra ppppppppppppppppppppppppppppppppppppppppppppp173 Reactive Oxygen Species in Plant Signaling Cezary Waszczak, Melanie Carmody, and Jaakko Kangasj¨arvi pppppppppppppppppppppppppp209 Cell and Developmental Biology of Plant Mitogen-Activated Protein Kinases Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org ˇ ˇ ppppppppppppppppppppp

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. George Komis, Olga Samajová, Miroslav Oveˇcka, and Jozef Samaj 237 Receptor-Like Cytoplasmic Kinases: Central Players in Plant Receptor Kinase–Mediated Signaling Xiangxiu Liang and Jian-Min Zhou pppppppppppppppppppppppppppppppppppppppppppppppppppppp267 Plant Malectin-Like Receptor Kinases: From Cell Wall Integrity to Immunity and Beyond Christina Maria Franck, Jens Westermann, and Aurélien Boisson-Dernier pppppppppppp301 Kinesins and Myosins: Molecular Motors that Coordinate Cellular Functions in Plants Andreas Nebenführ and Ram Dixit pppppppppppppppppppppppppppppppppppppppppppppppppppppppp329

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The Oxylipin Pathways: Biochemistry and Function Claus Wasternack and Ivo Feussner pppppppppppppppppppppppppppppppppppppppppppppppppppppppp363 Modularity in Jasmonate Signaling for Multistress Resilience Gregg A. Howe, Ian T. Major, and Abraham J. Koo ppppppppppppppppppppppppppppppppppppp387 Essential Roles of Local Auxin Biosynthesis in Plant Development and in Adaptation to Environmental Changes Yunde Zhao pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp417 Genetic Regulation of Shoot Architecture Bing Wang, Steven M. Smith, and Jiayang Li ppppppppppppppppppppppppppppppppppppppppppp437 Heterogeneity and Robustness in Plant Morphogenesis: From Cells to Organs Lilan Hong, Mathilde Dumond, Mingyuan Zhu, Satoru Tsugawa, Chun-Biu Li, Arezki Boudaoud, Olivier Hamant, and Adrienne H.K. Roeder pppppp469 Genetically Encoded Biosensors in Plants: Pathways to Discovery Ankit Walia, Rainer Waadt, and Alexander M. Jones ppppppppppppppppppppppppppppppppppp497 Exploring the Spatiotemporal Organization of Membrane Proteins in Living Plant Cells Li Wang, Yiqun Xue, Jingjing Xing, Kai Song, and Jinxing Lin ppppppppppppppppppppppp525 One Hundred Ways to Invent the Sexes: Theoretical and Observed PathstoDioecyinPlants Isabelle M. Henry, Takashi Akagi, Ryutaro Tao, and Luca Comai pppppppppppppppppppppp553 Meiotic Recombination: Mixing It Up in Plants Yingxiang Wang and Gregory P. Copenhaver pppppppppppppppppppppppppppppppppppppppppppp577 Population Genomics of Herbicide Resistance: Adaptation via Evolutionary Rescue Julia M. Kreiner, John R. Stinchcombe, and Stephen I. Wright ppppppppppppppppppppppppp611 Strategies for Enhanced Crop Resistance to Insect Pests Angela E. Douglas ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp637 Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org

Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only. Preadaptation and Naturalization of Nonnative Species: Darwin’s Two Fundamental Insights into Species Invasion Marc W. Cadotte, Sara E. Campbell, Shao-peng Li, Darwin S. Sodhi, and Nicholas E. Mandrak pppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp661 Macroevolutionary Patterns of Flowering Plant Speciation and Extinction Jana C. Vamosi, Susana Magall´on, Itay Mayrose, Sarah P. Otto, and Herv´e Sauquet ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp685

vi Contents PP69_FrontMatter ARI 5 April 2018 9:11

When Two Rights Make a Wrong: The Evolutionary Genetics of Plant Hybrid Incompatibilities Lila Fishman and Andrea L. Sweigart ppppppppppppppppppppppppppppppppppppppppppppppppppppp707 The Physiological Basis of Drought Tolerance in Crop Plants: A Scenario-Dependent Probabilistic Approach Fran¸cois Tardieu, Thierry Simonneau, and Bertrand Muller pppppppppppppppppppppppppppp733 Paleobotany and Global Change: Important Lessons for Species to Biomes from Vegetation Responses to Past Global Change Jennifer C. McElwain ppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppppp761 Trends in Global Agricultural Land Use: Implications for Environmental Health and Food Security Navin Ramankutty, Zia Mehrabi, Katharina Waha, Larissa Jarvis, Claire Kremen, Mario Herrero, and Loren H. Rieseberg pppppppppppppppppppppppppppppp789

Errata

An online log of corrections to Annual Review of Plant Biology articles may be found at http://www.annualreviews.org/errata/arplant Annu. Rev. Plant Biol. 2018.69:761-787. Downloaded from www.annualreviews.org Access provided by Universidad de Costa Rica (UCR) on 02/21/19. For personal use only.

Contents vii