Plant-Climate Interactions Over Historical and Geological Time

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Plant-climate interactions over historical and geological time

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Plant-climate interactions over historical and geological time

Sharon A. Cowling

Doctoral Dissertation Lund,2000 A doctoral thesis at a university in Sweden is produced either as a monograph or as a collection of papers. In the latter case, the introductory part constitutes the formal thesis, which summarizes the accompanying papers. These have either already been published or are manuscripts at various stages (i.e. in press, submitted, or manuscript). DISCLAIMER

Portions of this document may be illegible in electronic image products. Images are produced from the best available original document. Plant-climate interactions over historical and geological time

Sharon A. Cowling

Academic dissertation for the degree of Doctor of Philosophy, to be publicly defended in Bla Hallen at the Institute of Ecology, Plant Ecology (Solvegatan 37) on May 18th, 2000 at 10:00 am, by permission of the Faculty of Mathematics and Natural Sciences of Lund University. The thesis will be defended in English.

Faculty opponent

Professor I. Colin Prentice Max Planck Institute for Biogeochemistry Jena, Germany Document name LUND UNIVERSITY Institute of Ecology DOCTORAL DISSERTATION Plant Ecology Due 0/tee April 13, 2000 Lund University S223 62 Lund, Sweden CODEN: SE-LundBDS/NBBE-00/1058+216pp

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Abstract Data-model comparisons are a useful approach to elucidating the relative influence of past climate change on vegetation dynamics over various spatial (global, regional, stand) and temporal (historical, geological) scales. Comparisons between changes in tree species abundance reconstructed from pollen and simulated from a forest gap model, for example, indicate that based solely on climate change over the past 1500 years, southern Scandinavian forests should be co-dominated by Tilia and Fagus. Picea has begun to more closely track changes in climate since 1000 years ago, however in the last few centuries the realised range limit of Picea has overshot the potential limit because of planting and establishment during favourable years. Not only can palaeodata-modei comparisons provide practical information for forest managers, but they can help further our appreciation of the climatic catalysts underlying evolution of terrestrial ecosystems. Past changes in atmospheric CO2, independently or in combination with changes in climate, may have altered vegetation form and function such that palaeoplant assemblages were much different than today, speciation may have been promoted via biological vicariance, and some species may have been pushed to extinction. A thorough understanding of modern plant-climate interactions requires consideration of how past climate and atmospheric CO2 events could have shaped physiological, biochemical and biophysical functioning of existing vegetation.

^f plant-climate interactions, vegetation modelling, palaeoecology, plant evolution, atmospheric CO2

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Sharon A. Cowling (Institute of Ecology, Plant Ecology, Lund University, Sweden)

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Contents Page

1.0 Introductory summaries: 1.1 Historical changes in species composition by variations in climate 5

1.2 SA Cowling (2000) Overcoming our high CO2 research bias, manuscript 17

2.0 Acknowledgments 29

3.0 List of papers 33

I. SA Cowling, MT Sykes and RHW Bradshaw (2000) Palaeoforest data-model comparisons: evaluating tree succession in Scandinavia over the past 1500 years, submitted, Journal of Ecology.

II. RHW Bradshaw, B Holmqvist, SA Cowling, and MT Sykes (2000) The effects of climate change on the distribution and management of Picea abies in southern Scandinavia, submitted, Canadian Journal of Forestry.

III. SA Cowling (1999a) Simulated effects of low atmospheric CO2 on structure and composition of North American vegetation at the Last Glacial Maximum. Global Ecology and Biogeography 8, 81-93 *

IV. SA Cowling and MT Sykes (1999) Physiological significance of low atmospheric CO2 for plant-climate interactions. Quaternary Research 52, 237-242 ** V. SA Cowling and MT Sykes (2000) Reply: Do low CO2 concentrations affect pollen-based reconstruction of LGM climate? Quaternary Research 53 (in press) **

VI. SA Cowling, MA Maslin and MT Sykes (1999) A theory of allopatric speciation derived from palaeovegetation simulations of Amazonia. Quaternary Research (accepted, in revision).

VII. SA Cowling (2000) Carbon stress, evolutionary innovation and extinction in land plants, submitted, Global Change Biology.

VIII. SA Cowling (1999b) Plants and temperature-CO2 uncoupling. Science 285, 1500-1501***

IX. SA Cowling (2000) Rubisco adaptations to Pleistocene climate cycles. Manuscript (in revision).

* reprinted with permission from Blackwell Science Ltd. ** reprinted with permission from Academic Press, Inc. *** reprinted with permission from the American Association for the Advancement of Science

4.0 Appendices

4.1 Geological time scale (last 300 Ma) 211

4.2 List of Plant Ecology Ph.D. Theses 213 HISTORICAL CHANGES IN conducted at the regional or local SPECIES COMPOSITION BY scale (Solomon and Shugart VARIATIONS IN CLIMATE 1984, Davis and Botkin 1985, Campbell and Me Andrews 1993) Sharon A. Cowling and even fewer at the stand- scale, yet such comparisons can Climate Impacts Group provide important insights into Institute of Ecology the critical factors modifying Lund University local and landscape tree succession in response to changes in climate. Because APPLICATIONS OF MODEL-DATA forest models simulate the COMPARISONS FOR FOREST influence of changes in climate RESEARCH on forest succession in the absence of anthropogenic act- Paleodata-model comparisons are ivities like planting, selective- a critical component of global cutting, or introduction of graz- change research because factorial ing animals, they are also useful modelling experiments allow for isolating the independent interacting biotic and abiotic effects of climate from anthro- components to be isolated, and pogenic disturbances (PAPERS I their relative influence be &II). evaluated in terms of trends The accuracy and the observed in the paleorecord. usefulness of palaeovegetation- Most palaeovegetation model comparisons depend to a data-model comparisons to date great degree on the quality of have focused on the effects of climate data. Previous paleoclimate and atmospheric changes simulations have been conducted on times-scales of millennia or with paleoclimate reconstructed greater, and have helped to from pollen (Solomon et al. provide important information on 1981, Davis and Botkin 1985) past vegetation-climate feed- and static climatic parameters backs, low atmospheric CO2- averaged over several hundred plant interactions (PAPERS III- years (Campbell and McAndrews VI), and on the evolution of plant 1993). The former approach is systems in general (PAPERS limited because of the use of VII-IX). The success of these pollen to both reconstruct climate long-term and large-scale studies and compare with simulation lends support for their use in data (often described as circular more regional applications. reasoning), while the latter There are few examples of approach offers little in the way paleodata-model comparisons of temporal resolution. Thus far, no palaeoforest-model compar- the paleorecord can be assumed isons have been made based on to be caused only by changes in gap model simulations using climate. Once it has been paleoclimate reconstructions established that the forest model from tree-rings, which allow for and paleoclimate database are much finer temporal resolution robust enough to capture major than other palaeotemperature climate-induced changes in forest proxies. dynamics, applications for sites Retrospective applications in areas believed to have had a of gap models have up to now combination of climatic and centred on eastern North human influences is made America (Solomon et al. 1981, possible. Davis and Botkin 1985, Campbell and McAndrews 1993). Applications for Europe FOREST GAP MODELS AND are also relevant because of the FORSKA2 long history of human-forest interactions and because of the Disturbance of forests by wind current debate on the factors and fire creates opportunities for responsible for shaping the understorey species to compete European vegetation landscape for increased ground-level light (Behre 1988, Chambers 1993). in newly formed gaps. Models Palaeoecological and arch- incorporating forest gap-phase aeological research in southern dynamics were first introduced in Sweden, for example, show that the early 1980s and since then humans were already interfering have undergone modifications to with forested systems in remote offer more mechanistic regions of northern Europe by as representations of forest pro- early as 4000 BC (Berglund cesses (Bugmann and Cramer 1991,Berglundefa/. 1996). 1998). In addition to inter- In order for forest models species competition for light, to be effective in isolating abiotic water and other resources, forest and biotic influences on forest processes in gap models are succession, they must first be influenced by climate (temp- tested for their ability to capture erature, precipitation, sunshine), major trends in past tree hence they have become abundance (PAPER I). For model effective tools for predicting validations, therefore, sites forest responses to future climate which are known to have had warming (Prentice et al. 1991, minimal disturbance from Smith and Shugart 1996, Sykes humans must be selected, so that and Prentice 1996, Bugmann successional trends observed in 1997, Linder et al. 1997). One such example of a and in addition to random events, mechanistic forest model is is dependent on tree age. All FORSKA, which simulates the physiologically-based processes establishment, growth and (establishment, photosynthesis, mortality of trees in canopy gaps respiration) are subject to of approximately 0.1 hectare in environmental constraints (i.e. size (Leemans and Prentice 1989, growing-degree days, minimum Prentice et al. 1993). FORSKA and maximum temperatures, soil (and its later versions) has been drought index), which are used to simulate forests in calculated from mean monthly northern Europe (Prentice et al. climate. The robustness of 1991, Leemans 1992, Sykes and FORSKA in predicting fund- Prentice 1996), Canada (Price et amental stand dynamics in al. 1993), and tropical Africa northern temperate forests has (Desanker and Prentice 1994). been evaluated by Leemans and FORSKA2 (Prentice et al. 1993) Prentice (1987, 1989) and differs from earlier gap models in Leemans (1992). that it offers more realistic mathematical representations of competition for light, and HISTORICAL CHANGES IN contains more explicit tree NORTHERN EUROPEAN CLIMATE physiology-based parameters (such as the effects of temp- Over the past 1500 years, erature and drought on net northwestern Europe has photosynthesis and sapwood experienced three significant respiration). climate change events, evidenced Simulated tree establish- by a combination of meteor- ment and growth depend on ological, glacial, and tree-line favourable climate and solar retreat data (Grove 1994, Hughes radiation, and are also influenced and Diaz 1994, Frenzel 1996, by species-specific parameters Keigwin 1996), and include the such as shade-tolerance, estab- following: 1) a cold period pre- lishment rates and sprouting ceding the start of the Middle potential. Tree mortality in Ages sometimes referred to as FORSKA2 is modelled on the the Medieval Cold Period (MCP, basis of two functions; an AD 500-900), 2) an interval of intrinsic mortality rate correlated warmth during the Middle Ages with tree age and vigour, and termed the Medieval Warm random mortality resulting from Period (MWP, AD 900-1200), disturbances such as wind and and 3) a prolonged cold event fire. Disturbance is simulated by called the Little Ice Age (LIA, removal of tree cover in patches, AD 1200-1850). A 1500-year Scandinavian MODEL VALIDATION: paleoclimate database (PAPER I) PENNINGHOLMEN CASE-STUDY was constructed using a combination of palaeotemperature Penningholmen was chosen as a anomalies reconstructed from case-study to validate Fennoscandia tree-rings (Briffa FORSKA2's performance in et al 1992) and palaeo- simulating forest succession over precipitation anomalies from the past 1500 years (PAPER I) historical documents (Lamb, because its remote, northerly 1967). The application of location in the Swedish Lapland northern data to southern Scan- suggests that it was likely dinavia is supported by the minimally disturbed by humans observation that major northern for most of the past 1500 years temperature anomalies are (apart from the present century). duplicated in shorter datasets Penningholmen is a small (0.9 from further south (Kalela- ha) island in Lake Uddjaure, Brundin 1999). dominated by Betula pubescens, The Scandinavian paleo- Picea abies and Pinus sylvestris, climate database indicates that and lies approximately 300 m 30-year mean temperatures below the forest-tundra ecotone during the MWP were up to and close to the northwestern 0.5°C greater than today, with a range limits of Picea abies and general warming trend beginning Pinus sylvestris. by AD 900 and ending by AD A comparison of simulated 1200. The LIA is a longer period percent Betula and Pinus of cooling (AD 1200-1850), biomass (defined as the punctuated by one major proportion of species biomass warming event starting AD 1400. relative to total forest biomass) LIA temperatures reached a and observed changes in forest maximum cooling around AD pollen percentages indicates that 1600 with a 30-year mean FORSKA2 adequately captures anomaly of 0.7°C decrease major successional trends over relative to today. the past 1500 years. Both MWP precipitation was simulation and observational generally greater in the winters data indicate that Pinus (by 7%) and less in the summers experiences two periods of lower (by 17%). In contrast, LIA win- abundance; declines culminating ters were drier (5-10%) and at AD 1050 (i.e. MWP) and AD summers were variable, but 1650 (i.e. late-LIA). Similarly, tending towards wetter. simulated and observed trends in Betula show one major period of decreased abundance, during the MODEL COMPARISONS TO early part of the LIA. SOUTHERN SCANDINAVIA Penningholmen lies quite close to the northwestern range Much debate focuses on the limits of Pinus sylvestris, origins of beech forests in therefore the simulated and Europe, primarily owing to its observed decline in Pinus during current dominance of forest the most coldest period of the stands across large areas of LIA may be related to an central and northern Europe, but eastward contraction of the also because in many countries, western Pinus species limit. beech forests are valued ancient Kullman (1987, 1988) also landscapes (Brunet 1995, Kuster reports a contraction of the most 1997, Peters 1997, Rackham northerly limit of Pinus in the 1997). A widely held opinion in central Scandes mountains at this northwest Europe is that beech time. forests are natural components of Although Bradshaw and the landscape, a notion re- Zackrisson (1990) suggest that inforced by publications citing the observed dieback of Betula historical descriptions of the during the first half of the LIA existence of beech forests 300 to was related to insect herbivory, it 400 years ago (Brunet 1995, may also be related to the effects Ellenberg 1996, Bjorkman 1997). of LIA climate on competitive Fagus sylvatica is most interactions between Pinus and likely in equilibrium with climate Betula. This hypothesis is based on the continental-scale (Huntley on simulation data, which also et al. 1989), however palaeo- shows trends towards lower ecological investigation of Betula abundance during the sediments in small forest hollows early LIA. The role of in southern Sweden (Bjorkman palaeoforest data-model compar- and Bradshaw 1996, Bjorse and isons in separating the com- Bradshaw 1996) indicate pounding influences of abiotic dramatic increases in Fagus (climatic) and biotic (i.e. populations (at the expense of herbivory) factors on vegetation Tilia) starting around AD 1600. dynamics is strongly highlighted These records show that 1500 in these data-model comparisons years before present, forests were (PAPER I). co-dominated by Fagus (beech) and Tilia (lime), therefore from a paleoecological-perspective, pure THE BEECH-LIME STORY: Fagus woodlands may not APPLYING PALEOFOREST DATA- necessarily be a 'natural' feature of the Scandinavian landscape (Kuster 1997, Bradshaw and 1962, Berglund 1966). Holmqvist 1999). Palaeoforest FORSKA2 simulations support data-model comparisons may be the theory that factors other that helpful for addressing this issue LIA cooling must be responsible because they can help determine for Tilia's near disappearance if changes in climate associated from southern Scandinavia with the Medieval Warm Period (PAPER I). Natural pathogenic and the Little Ice Age might have and anthropogenic factors such had an effect on Tilia and Fagus as selective-cutting, large-scale competition and succession. forest clearance for agriculture FORSKA2 simulations do and introduction of grazing not support the hypothesis that animals could have resulted in historical changes in climate smaller than expected pop- were favourable for stand-scale ulations of Tilia. dominance of beech, and indicate Paleorecords show no that after the termination of LIA evidence of pathogenic decline, cooling, Tilia tree populations while selective-cutting seems should have re-established their unlikely, as Tilia was historically initial dominance in nemoral used as an important fodder woodlands (PAPER I). Seed species (Behre 1988). Large- production in Fagus is reduced scale forest clearance for when the number of warm agriculture would probably have growing-degree days decreases enhanced Tilia''s establishment (Peters 1997), therefore a de- potential because of its crease in Fagus abundance proliferation by stump sprouting during the LIA is an expected (Aaby 1986). simulation response. Since Tilia On the other hand, field is capable of reproducing veget- studies show that Tilia is atively, it can persist on sites preferentially selected by deer, even in the face of colder and moose and domesticated live- unfavourable climate (Prentice stock, while Fagus is least and Helmisaari 1991). Examples preferred, prompting Nilsson where Tilia individuals have re- (1987) to conclude that grazing mained in areas with un- animals have played a more favourable climate for up to important role in altering several centuries, have been Swedish boreonemoral forest noted for northern Europe (Pigott succession than late-Holocene andHuntley 1981). climate change. It should be The weak presence of Tilia noted, however, that F0RSKA2 has been a long-standing charac- simulations indicate that Tilia teristic of forests in northwest was already starting to decline as Europe (Iversen 1958, Turner a result of LIA cooling when

10 human disturbance began inten- palaeovegetation maps to static sifying, thus a scenario where and dynamic bioclimatic sim- Tilia populations were weakened ulation models indicates that the by LIA cooling and made more range limit of Picea has begun to susceptible to grazing by live- track climate change during the stock, can also be hypothesised last 1000 years more closely than (PAPER I). in the past (PAPER II). Data- model comparisons of the spread of Picea into southern Scan- FUTURE TEMPERATURE WARMING dinavia show that the mapped AND FOREST DYNAMICS: THE range lagged the potential range MWP ANALOGY by c. 100 km 1000-500 years ago. The Medieval Warm Period In contrast, the realised (MWP) was a well-documented range limit of Picea has ap- climate anomaly event occurring proached the potential range between AD 900 and AD 1100, limit and overshot during the last but was primarily experienced few centuries as a result of only in the Northern Hemisphere planting and establishment dur- (Hughes and Diaz 1994). ing climatically favourable years. FORSKA2 simulations indicate Future predictions suggest that cooling associated with the that Picea's range will retreat Little Ice Age was more im- northwards, and outlying pop- portant for forest dynamics in ulations will be out of Scandinavia than MWP warm- equilibrium with climate and ing. Warming of approximately under threat to environmental 0.5°C led to a small decline in stress (PAPER II). We suggest Pinus populations in northern that when a species is expanding Sweden, with a slight increase in its range, migrational lag may "deciduousness" (i.e. Fagus and operate when expansion is rapid, Tilia abundances) in the south but during range contraction or (PAPER I). the rare periods of stability, the potential and realised ranges overlap more closely. Our conclusion has CLIMATE CHANGE AND PICEA: implications for forestry in IMPLICATIONS FOR MANAGEMENT southern Scandinavia. There are risks involved in the cultivation Picea is the most of species close to and beyond important commercial species in their distributional limits, es- Scandinavia. A recent study pecially during periods of rapid incorporating comparisons of climate change. Storm damage is

11 one way in which climatic con- applications, including the trol may operate, but other investigation of climate versus physiological weaknesses are migrational control on past tree also possible. Our over-riding species limits, prediction of conclusion, therefore, is that we future species limits for forest advise against promoting Picea species of economic importance monocultures in southern Scan- (e.g. Pinus, Picea, Quercus), the dinavia at any time during the identification of potential bio- foreseeable future (PAPER II). logical migrational barriers, and reconstructions of paleoclimate based on inverse modelling. Veg- etation modelling in combination THE FUTURE OF PALAEOFOREST with paleoecological data has MODELLING and will continue to expand the scope of forest research by One of the major limitations to providing a highly innovative gap models in general, and and flexible investigative tool. F0RSKA2 in particular, is that processes of seed dispersal and migration are not mechanistically modelled. Instead, migration is REFERENCES simulated by a user-defined parameter which specifies Aaby, B. 1983. Forest whether seeds of a species are development, soil genesis and available or not for planting. human activity illustrated by Mathematical algorithms pollen and hypha analysis of two describing the physiological and neighbouring podzols in Draved silvicultural processes involved Forest, Denmark. Danm. Geol. in migration will be necessary for Unders.II 114:1-114. more advanced palaeoforest data- model applications. A migration Behre, K. 1988. The role of man module was not developed for in European vegetation history. FORSKA2 because a more ap- Pages 633-672 in B. Huntley and propriate vegetation model, one T. Webb III., editors. Vegetation incorporating biogeochemistry history. Kluwer Academic and species-level dynamics sim- Publishers, Dordrecht. ulated at the level of the landscape, has just recently been Berglund, B.E. 1966. Late- developed (Smith et al. 2000). Quaternary vegetation in Eastern Such regional vegetation- Blekinge, southeastern Sweden. forest models can be effectively A pollen-analytical study. II. employed for a variety of new

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16 OVERCOMING OUR HIGH CO2 RESEARCH BIAS If trends in atmospheric CO2 reconstructed for the past four Sharon A. Cowling interglacial-glacial cycles (10) are typical for most of the Institute of Ecology Pleistocene (1.6 Ma), then late- Lund University Cenozoic vegetation has existed Sweden in low CO2 conditions (around 200 umol mol'1) for approximately ten times as long 1 Atmospheric CO2 concentrations as in high CO2 (280 umol mol" ). have fluctuated greatly over the Based on the length of time of history of the Earth (1) and are low CO2 glacials alone, modern- likely to continue to do so in the day C3-plants should likely still face of enhanced CO2 release show features of low CO2 from fossil fuel burning and adaptation (11). Three lines of deforestation. With reason, physiological and biochemical much important research focuses research support this hypothesis. on understanding and predicting First, little evidence plant responses to changes in indicates that plants can atmospheric CO2 (2-8). photosynthetically acclimate A cursory assessment of ('up-regulate') low CO2 by either published papers on CO2-plant increasing activity or content of interactions reveals that elevated Rubisco, the primary CO2 studies out-number low CO2 carboxylating enzyme in C3- papers by over four-fold (9). plants (12-16). Although high CO2 research is Moreover, plants exposed arguably critical for addressing to doubled CO2 (in the absence future global change issues, to of root restriction or nutrient what extent do these studies deficiencies) tend to show down- contribute to our understanding regulation of photosynthesis due of the fundamental processes and to source-sink feedbacks (often a mechanisms underlying plant build-up of starch in the responses to environmental chloroplast which in turn change? In other words, is our damages the light-harvesting elevated CO2 research bias system) (17-21). Down- justified in the interest of regulation in response to furthering basic plant sciences? relatively higher CO2 concentrations, together with an absence of acclimation to low

LOW CO2 ADAPTATIONS IN CO2, strongly indicates that C3- MODERN-DAY PLANTS

17 plants are biochemically fine- showed marked responses to tuned to the low CO2 condition. atmospheric carbon-depletion: Last, plants tend to show 1) As a result of low-CO2- an inherent conservatism in the induced reductions in plant way that carbohydrates are water-use efficiency (WUE), allocated to storage (11). Rather tropical alpine treelines than prematurely undergoing probably migrated downslope senescence, plants subject to (23), creating hybrid-zones of carbon-depleting environmental mixed lowland-highland stresses like high temperatures species (24). and low atmospheric CO2 reduce 2) Many glacial plant growth, but maintain labile assemblages were much carbohydrate pools similar to that different than those today (25, under (non-stressed) control CO2 26), probably as a result of conditions (22). The ability of CO2-induced changes in modern-day plants to conserve WUE (27) (PAPER III) and in carbon balance under various changes to photo-synthetic environmental stresses may be a thermal optima (i.e. growth feature carried over from times optima) (PAPERS IV and V). when carbon was much more 3) Competition between glacial limiting (11). C3- and C4-plants was probably altered such that C4- dominated ecosystems ex- EVOLUTION OF PLANT-CARBON panded at the expense of C3- FITNESS systems (31-33). 4) Species gene pools may have What event or culmination of become isolated in forest events could have catalyzed the and/or canopy refugia, evolution of 'carbon-fitness' inducing allopatric speciation, (defined in the context of this and helping to explain paper as being the basic ability of modern patterns of tropical plants to compensate for low endemism (PAPER VI). carbon balance)? The Pleist- Although vegetation likely ocene, the most recent geological responded significantly to period characterized by frequent lowered glacial atmospheric CO2, low CO2 events, is an obvious there were surprisingly few plant starting point. extinctions during the We can infer from a Pleistocene (35). Plant genotypes combination of factorial model- surviving to the Pleistocene ling experiments and palaeo- probably had already been vegetation data that glacial plants selected for carbon-fitness during were sensitive to low CO2 and earlier periods of carbon-stress.

18 Streamlining of features of plant imbalances (PAPER VII). The carbon-fitness, therefore, likely warming and relatively low CO2 began before the Pleistocene, event in the Miocene (45) may possibly as early as the start of have held critical consequences the Cenozoic (PAPER VII). for the Earth's flora, in that it Palaeotemperatures over was an important catalyst for the the Paleocene-Eocene transition proliferation of plants having the are assumed to be forced by C4-photosynthetic syndrome (46) atmospheric CO2, although (PAPERS VII and VIII). recent research (37-40) now identifies methane as an important temperature-forcing IMPLICATIONS FOR UNDER- agent. If methane released from STANDING ANCIENT AND MODERN ocean hydrates was the primary PLANT FUNCTION driver of terminal-Paleocene warming (one of the Earth's last If we adopt the perspective that greatest warming phases), baseline plant responses to biotic atmospheric CO2 may not have and abiotic factors have a been as high as previously foundation in low CO2 suspected (41). The combination adaptations, then much of what of very high temperatures and we've reconstructed of past relatively low atmospheric CO2 plant-environment interactions, (both contributing to increased and how we interpret the photorespiratory carbon loss) function of current plant may have placed early-Cenozoic processes, may also have to be plants under conditions of high reconsidered (PAPER IX). carbohydrate stress (PAPER Theoretical reconstruc- VIII), thereby forcing selection tions of photosynthesis in ancient of plant genotypes on the basis of plants (48) may be biased their ability to overcome extreme because of the assumption that fluctuations in plant carbon the primary biochemical balance (PAPER VII). limitations to C3-photosynthesis Decreases in plant in earlier plants (i.e. Rubisco, diversity (43) and increases in electron-transport, and end- insect herbivory (44) recon- product utilisation) (49) were of structed from the Paleocene- the same strength and relative Eocene fossil record may not importance as those in modern- only be correlated with climate day plants. warming, but probably more Photo synthetic limitations directly to the failure of certain arising from electron-transport plant genotypes to sufficiently and/or source-sink feedbacks are overcome imposed carbon probably much stronger in plants

19 today than during earlier periods modelled for ancient plant of high CO2 (e.g. the systems (48, 59). Cretaceous), because strong Such applications are Rubisco limitations during low possible only if we adopt the CO2 glacials may also have following three assumptions, resulted in the selection of although in many cases, these genotypes having strong non- assumptions are not explicitly Rubisco limitations (PAPER IX). identified. Photosynthesis is most efficient 1. Modern-day plants are fully- when the rates of biochemical adapted to pre-Industrial CO2 limitations are adjusted so that no concentrations, so that the one step is solely limiting to relationship between stomatal carbon-uptake (49, 50). index and (pre-Industrial) An alternative approach to CO2 can be used as a standard understanding the functioning of for reconstructing ancient ancient ecosystems may be to atmospheric CO2 levels. perform sensitivity-analysis 2. There is a direct relationship modelling experiments to de- between changes in stomatal termine what possible com- index and stomatal conduc- bination of photosynthetic tance. limitations would have allowed 3. Ancient plant systems tracked Cretaceous plants (for example) changes in atmospheric CO2 to have grown to the extent that for the same functional reason is indicated in the fossil record. as they do today. Perhaps one of the most Empirical data presented critical implications of assuming in this article and elsewhere (60), that baseline plant functions are indicate that modern-day plants influenced by low CO2-plant are not adapted to interglacial interactions concerns our CO2 levels, and that stomata do understanding of the relationship not acclimate to high CO2 (60). between leaf (stomatal) Therefore, the relationship properties and atmospheric CO2. between glacial stomatal index Empirical studies show a direct and glacial CO2 (as relationship between CO2 and the reconstructed from ice core data) ratio of stomatal to epidermal would probably provide a more cells (called stomatal index) (51- appropriate standard for 54), which has resulted in past reconstructing ancient CO2 changes in atmospheric CO2 to levels, than the current practice be reconstructed from differences of using modern-day (pre- in stomatal index in fossil leaves Industrial) analogues. (56-58), and in rates of photo- Few studies have synthetic carbon-uptake to be investigated the correlation

20 between changes in stomatal current changes in atmospheric index and stomatal conductance CO2 are probably constrained by (60), but what few have been plant adaptations to low CO2, performed, generally indicate such that a 'ceiling' is placed on little correlation (61). Because it the responsiveness of stomatal is possible to test this index to increases in CO2 (62), to assumption, and because this is ensure that plants will be able to such a critical assumption for rapidly respond to declining CO2 many stomatal index-CO2 concentrations at the start of the applications, increased effort next glaciation. If these should be placed on conducting suggested caveats prove more more of these types of realistic than the current set of experiments. assumptions, then the use of Although the last stomatal-CO2 relationships to assumption is difficult to trace changes in CO2 may not be address, it raises some important so applicable for periods earlier issues on the nature and function than the Pleistocene, like for of stomatal-CO2 relationships. example the Mesozoic (63). From simply the perspective of plant energy and carbon conservation, it would be far CONCLUSIONS more important that plants be able to respond to (and trace) I do not advocate reducing the decreases in atmospheric CO2, quantity of high CO2 research (as than increases in CO2. If plants the importance of these are unable to adjust stomatal experiments is clearly properties in response to recognised), but rather to relatively high CO2, then one can highlight the need for more imagine few deleterious studies aimed at addressing low consequences for plant carbon CO2-plant interactions. Because economy. The same cannot be evidence points toward existing said for the inability of plants to adaptations to low CO2 in respond to decreases in modern-day plants, experiments atmospheric CO2. designed to help us understand If stomatal-tracking of basic plant form and function CO2 is only really important for may be best conducted under periods of low CO2, then perhaps CO2 levels more indicative of the strong correlation observed the Pleistocene period as a between stomatal index and CO2 whole. is a distinctly Pleistocene This article was also phenomena. The ability of written with the intent to modern-day plants to trace emphasise the value of looking at

21 modern-day physiological 6. Field, C.B., Lund, C.P., questions from a more geological Chiariello, N.R. and perspective, and to stress that the Mortimer, B.E. (1997) CO2 Pleistocene may not only have effects on the water budget been a unique period in the of grassland microcosm evolution of the Earth's climate communitites. Glob. Change system, but also an important Biol. 3, 197-206. event in the evolution of 7. Korner, C. (1998) Tropical terrestrial ecosystems. forests in a CO2-rich world. Clim. Change 39,297-315 8. Malhi, Y., Baldocchi, D.D. NOTES AND REFERENCES and Jarvis, P.G. (1999) The carbon balance of tropical, 1. Raymo, M.E. (1992) Global temperate and boreal climate change: a three forests. Plant Cell Environ. million year perspective. 22,715-740 Start of a Glacial (eds. G.J. 9. A literature survey was Kukla and W. Went), pp. 207- conducted using the Institute 223. Springer-Verlag, Berlin. for Scientific Information 2. Long, S.P. (1991) (ISI)'s citation database. The Modification of the response search was performed using of photosynthetic the 'Science Citation Index productivity to rising expanded' option, which temperature by atmospheric incorporates publications CO2 concentrations: has its from 1986 to the present. Of importance been under- 10,425,207 publications listed estimated? Plant Cell in the database, 1825 hits Environ. 14, 729-739 were recorded for the 3. Amthor, J.S. (1991) keyword 'elevated CO2' and Respiration in a future, 423 hits for the keyword 'low higher CO2 world. Plant CO2\ Cell Environ. 14, 13-20 10. Petit, J.R. et. al. (1999) 4. Friend, A.D. and Cox, P.M. Atmospheric history of the (1995) Modeling the effects past 420,000 years from the of atmospheric CO2 on Vostok ice core, Antarctica. vegetation-atmosphere Nature 399, 429-436 interactions. Agr. For. 11. Sage, R.F. and Cowling, S.A. Meteorol. 73,285-295 (1999) Implications of 5. Farquhar, G.D. (1997) stress in low CO2 Carbon dioxide and atmospheres of the past: are vegetation. Science 278, today's plants too 1411 conservative for a high CO2

22 world? Carbon Dioxide and systems. Science 257, 1672- Environmental Stress (eds. Y. 1675 Luo and H.A. Mooney), pp. 18. Read, J.J., Morgan, J.A., 289-308. Academic Press, Chatterton, N.J., and San Diego. Harrison, P.A. (1997) Gas 12. Campbell, W.J., Allen, L.H., exchange and carbohydrate and Bowes, G. (1988) and nitrogen concentrations Effects of CO2 concen- in leaves of Pascopyrum tration on Rubisco activity, smithii (C-3) and Bonteloua amount and photosynthesis gracilis (C-4) at different in soybean leaves. Plant carbon dioxide concen- Physiol. 88, 1310-1316 trations and temperatures. 13. Sage, R.F. and Reid, CD. Ann. Bot. 79, 197-206 (1992) Photosynthetic 19. Cheng, S.H., Moore, B.D. and acclimation to sub-ambient Seeman, J.R. (1998) Effects CO2 (20 Pa) in the C3 of short- and long-term annual, Phaseolus vulgaris elevated CO2 on the L. Photosynth. 27, 605-617 expression of ribulose-1,5- 14. Sage, R.F. (1994) bisphosphate carboxylase/ Acclimation of photo- oxygenase genes and synthesis to increasing carbohydrate accumulation atmospheric CO2: the gas in leaves of Arabidopsis exchance perspective. thaliana. Plant Physiol. 116, Photosyn. Res. 39, 351-368 715-723 15. Johnson, H.B., Polley, H.W., 20. Moore, B.D., Cheng, S.H., and Mayeux, H.s. (1993) Rice, J. and Seemann, J.R. Increasing CO2 and plant- (1998) Sucrose cycling, plant interactions: effects Rubisco expression, and on natural vegetation. prediction of photosynthetic Vegetatio 104/105, 157-170 acclimation to elevated 16. Tissue, D.T., Griffin, K.L., atmospheric CO2. Plant Cell Thomas, R.B., and Strain, Environ. 21, 905-915 B.R. (1995) Effects of low 21.Wurth, M.K.R., Winter, K. and elevated CO2 on C3 and and Korner, C. (1998) Leaf C4 annuals. II. Photo- carbohydrate responses to synthesis and leaf bio- CO2 enrichment at the top chemistry. Oecologia 101, of a tropical forest. Oecol. 21-28 116, 18-25 17. Korner, C. and Amone, J.A. 22. Cowling, S.A. and Sage, R.F. (1992) Responses to (1998) Interactive effects of elevated carbon-dioxide in low atmospheric CO2 and artificial tropical eco- elevated temperature on

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24 Stable carbon and oxygen thermal max-imum. Science isotopes of pedogenic 286, 1531-1533 carbonates, Ajo Mountains, 39. Pearson, P.N. and Palmer, southern Arizona: implic- M.R. (1999) Middle Eocene ations for palaeo- seawater pH and atmos- environmental change. pheric carbon dioxide Paleogeogr. Palaeoclimat. concentration. Science 284, Palaeoecol. 124, 233-246 1824-1826 34. Cowling, S.A., Maslin, M.A. 40. Norris, R.D. and Rohl, U. and Sykes, M.T. (2000) A (1999) Carbon cycling and theory of allopatric the chronology of climate speciation based on warming during the palaeovegetation simul- Paleocene-Eocene trans- ations of Amazonia. Quat. ition. Nature 401, 775-778 Res. (in press) 4].Berner, R.A. (1994) 35. Potts, R. and Behrensmeyer, GEOCARBII: A revised A.K. (1992) Late-Cenozoic model of atmospheric CO2 terrestrial ecosystems. over Phanerozoic times. Terrestrial Ecosystems Amer. J. Sci. 29A, 56-91 Through Time (eds. 42. Cowling, S.A. (1999) Behrensmeyer A.K., Damuth, Perspectives: Paleoecology. J.D., DiMichele W.A., Potts, Plants and temperature- R., Sues, H., Wing, S.L.), pp. CO2 uncoupling. Science 419-542. University of 285, 1500-1501 Chicago Press, Chicago. 43. Wing, S.L., alroy, J. and 36. Cowling, S.A. (2000) Hickey, L.J. (1995) Plant Carbon stress, evolutionary and mammal diversity in innovation and extinction in the Paleocene to early land plants, submitted, Glob. Eocene of the Bighorn Change Biol. basin. Paleogeog. 37. Bains, S., Corfield, R.M., and Paleoclimatol. Paleoecol. Norris, R.D. (1999) 115,117-155 Mechanisms of climate 44. Wilf, P. and Labandeira, C.C. warming at the end of the (1999) Response of plant- Paleocene. Science 285, 724- insect associations to 727 Paleocene-Eocene warming. 38.Katz, M.E., Pak, D.K., Science 284, 2153-2156 Dickens, G.R. and Miller, 45.Pagani, M.A., Arthur, MA. K.G. (1999) The source and and Freeman, K.H. (1999) fate of massive carbon input Miocene evolution of during the latest Paleocene atmospheric carbon di-

25 oxide. Paleoceanogr. 14, 53. Bettarini, I., Vaccari, F.P., 273-292 Miglietta, F. (1998) 46. Ehleringer, J.R., Ceding, T.E. Elevated CO2 concentra- and Helliker B.R. (1997) C4 tions and stomatal density: photosynthesis, atmospheric observations from 17 plant CO2 and climate. Oecologia species growing in a CO2 112,285-299 spring in central Italy. 47. Cowling, S.A. (2000) Photo- Glob. Change Biol. 4, 17-22 synthetic adaptations to 54. Woodward, F.I. and Kelly, Pleistocene climate cycles. C.K. (1995) The influence Manuscript (in revision) of CO2 concentration on 48. Beerling, D.J. (1994) stomatal density. New Modelling paleophoto- Phytol. 131,311-327 synthesis: late-Cretaceeous 55. McElwain, J., Mitchell, FJ.G. to present. Phil. Trans. R. and Jones, M.B. (1995) Soc. London. B 346, 421-342 Relationship of stomatal 49. Farquhar, G.D., von density and index of Salix Caemmerer, S. and Berry, J.A. cinerea to atmospheric (1980) A biochemical model carbon dioxide concen- of photosynthetic CO2 trations in the Holocene. assimilation in leaves of C3 Holocene 5, 216-219 species. Planta 149, 78-90 56. McElwain, J.C. (1998) Do 50. Sage, R.F. and Reid, CD. fossil plants signal palaeo- (1994) Photosynthetic res- atmospheric CO2 concen- ponse mechanisms to tration in the geological environmental change in C3 past? Phil. Trans. R. Soc. plants. Plant-Environment London. B 353, 83-96 Interactions (ed. R.E. 57. Beerling, D.J., Chaloner, Wilkinson), pp. 413-499. W.G., Huntley, B., Pearson, Marcel Dekker Inc, New A. and Tooley, M.J. (1991) York. Tracking stomatal densities 51. Woodward, F.I. (1987) through a glacial cycle: Stomatal numbers are their significance for sensitive to increases in CO2 predicting the response of from pre-industrial levels. plants to changing atmos- Nature 327, 617-618 pheric CO2 concentrations. 52. Woodward, F.I. and Bazzaz, Glob. Ecol. Biogeogr. Lett. 1, F.A. (1988) The responses 136-142 of stomatal density to CO2 58. Wagner, F. Bohncke, S.J.P., partial pressures. J. Exp. Dilcher, D.L., Kurschner, Bot. 39, 1771-1781 W.M., van Geel, B., Visscher, H. (1999) Century-scale

26 shifts in early Holocene atmospheric CO2 concentration. Science 284, 1971- 1973 59. Beerling, DJ. and Woodward, F.I. (1997) Changes in land plant function over the Phanerozoic: reconstructions based on the fossil record. Bot. J. Linn. Soc. 124, 137-153 60. Morison, ILL. (1998) Stomatal response to increased CO2 concentration. J. Exp. BotA9, 443- 452 61.Berryman, C.A., Eamus, D. and Duff, G.A. (1994) Stomatal response to a range of variables in two tropical tree species grown with CO2 enrichment. J. Exp. Bot. 45, 539-546 62. Beerling, D.J. and Chaloner, W.G. (1993) Evolutionary responses of stomatal density to global CO2 change. Biol. J. Linn. Soc. 48,343-353 63. McElwain, J.C., Beerling, D.J., and Woodward, F.I. (1999) Fossil plants and global warming at the Triassic-Jurassic boundary. Science 285, 1386-1390

27 ACKNOWLEDGEMENTS I consider myself extremely lucky to have met such a large I have so many people to number of great scientists over acknowledge, both professionally the past few years. I would like and personally, so without delay to acknowledge the following let's begin... researchers for reviewing my manuscripts, engaging in lively First and foremost, I want to conversation, and for generally express my overwhelming providing a stimulating gratitude for my two supervisors, environment for academic Martin Sykes and Richard pursuits (listed in the order that Bradshaw, for allowing me I've met you...): Graham freedom to develop my ideas, Farquhar, Ian Woodward, Harold assisting me with academic, Bugman, AI Solomon, Bjorn logistic and administrative Berglund, Shinya Sugita, Marie- problems, and for being great Jose Gaillard, Andrew Friend, guys to boot! Without them, I Wolfgang Cramer, Brian can fairly confidently say that I Huntley, Thomas Stocker, Andre wouldn't have nearly perished on Berger, Mark Maslin, Nathalie de a Swiss mountainside (Martin is Noblet, Paul Valdes, Alayne soon to publish his book, "101 Street-Perrott, Roger Pielke, Guy ways to kill off your graduate Midgley and Scott Wing. student"), nor be able to trace my lingering Lyme disease ..and to those I've unfortunately symptoms to an excursion with not had the opportunity to meet, Richard to Draved Forest. but who have recently provided Thank-you both for this and so suggestions on my manuscripts: much more! Mark Pagani, Tom Web, and Mark Bush. Although not one of my official supervisors on paper, but most Thank-you to past teachers for assuredly one in spirit, I thank inspiring me with their Colin Prentice for his endless enthusiasm and interest in their supply of patience, under- research... RB Lee (physics), standing, generosity and Tony Davis (biogeography), inspiration. When seething from Larry Band (hydrology), Terry some ridiculous (!!) review, Blake (tree physiology), Grant there's no one who can placate Henderson (geology) and me and make me laugh as easily especially to Bob Jefferies and and quickly as Colin. Cheers, Dave Wedin (ecology). Tack and Danke!

29 Bo Wall en, thank you ever so I want to thank all my past, much for your enthusiastic present and future mentors, who support of my research and for by their example as brilliant your understanding and assis- scientists AND generous people tance from day-one. are reason enough to tolerate the nonsense associated with being a Acknowledgements go out to junior and female scientist. Bengt Nihlgard and the SUFOR Without you, I wouldn't be here project for funding and guidance. today... Cheers to those who smiled when Thank you to my students for I bumped into them in the constantly reminding me how hallways; in particular, Siv, exciting it can be in science. Lina Ragnhild, Irene, Maj-Britt, Mercado, congratulations on Birgitta and Anita. A special your MPI PhD position (!!), and note to Siv who tried to teach me best wishes to Daniel Jinnefalt Swedish, realised how hopeless I and Helena Martensson. was, and then teased me about it anyways. For technical, computer and administrative assistance, I I've left acknowledgments to would like to thank Kurt, family and friends until the end, Tommy, Inger, and Hakan. not because they are in any way, shape or form less important than Very special thank-you's go out professional ones, but because by to fellow CIG members: Torben listing them last I can gush with Christensen, Anna Joabsson, less fear of embarrassment (who Stephen Sitch, Jed Kaplan, reads acknowledgments to the Thomas Hickler, Ben Smith, and end anyways?!?). Justin Travis, as well as to visitors to our lab; Bjorn With that said, warm and Holmqvist, Anna Brostrom, Jack affectionate thank-you's go out Williams, Jian Ni, and Chunyin to: Liu. * Teresa for sticking with me over the long-haul (28-years and The staff at the Ekologihuset counting...) Bibliotek: Ase, Kristina, Bodil, * Ursula for maintaining my Shalini and Carola provided sanity and providing perspective service above and beyond the with hours of silly laughter call of duty. Thank-you all for * James, Wendy, Alannah, your assistance. Andrea, and Greg for keeping in

30 touch and reminding me what * Uncle Bill and Aunt Vivi for good friends are for... being who they are and for * Lesley and Laura for surviving taking their role of Mom and Dad the 'trapped-in-bus-for-10-hours- #2 so whole-heartedly during-windstorm' ordeal, and making me laugh about it I would like to dedicate my afterwards doctoral thesis to: * Andrew for his spontaneous, smile-provoking emails 1) my Grandma (Bernadette * new friends Katia, Asa, Paquet-Soltermann, -1998), Dagmar, Louise, Rene, Birgit, Grandpa (Rene Soltermann, Fredrik, Katja and Adolf -1999) and Grandpa (Harry Cowling, 1910-2000), in A Purple Heart for bravery is due memory of your spirited lives my family in recognition of their 2) my role-models; my Mom 1) tolerance of my whingeing, 2) (Carol Soltermann-Cowling), unchecked enthusiasm for my my Aunt Vivi (Vivian career choices, and 3) persistence Soltermann-Burgess) and my in keeping abreast of my latest Grandma (Bernadette Paquet- research project, despite the fact Soltermann). You've demon- that they never let me forget that strated by way of example I'm just a science geek with a that strength, courage, deter- childish sense of humour. Mom, mination, and independence is Dad, Brian and Gary - you mean the formula for success and the world to me !!! happiness in life.

Love, kisses and hugs to: So to summarise... * Melissa and Heather for being courageous enough to join the Gracias. Merci. Tack. Danke. Cowling Clan and for one day Thank-you. providing me with adorable, little nieces and nephews (now how's that for pressure?!)

* Grandma Cowling for following my travels with great interest and accepting that my page in her address book will be forever changing

31 Papers included in the thesis

I. SA Cowling, MT Sykes and RHW Bradshaw (2000) Palaeoforest data- model comparisons: evaluating tree succession in Scandinavia over the pastl500 years, submitted, Journal ofEcology.

II. RHW Bradshaw, B Holmqvist, SA Cowling, and MT Sykes (2000) The effects of climate change on the distribution and management ofPicea abies in southern Scandinavia, submitted, Canadian Journal of Forestry.

III. SA Cowling (1999a) Simulated effects of low atmospheric CO2 on structure and composition of North American vegetation at the Last Glacial Maxi- mum. Global Ecology and Biogeography8, 81-93.

IV. SA Cowling and MT Sykes (1999) Physiological significance of low atmospheric CO2 for plant-climate interactions. Quaternary Research 52, 237-242.

V. SA Cowling and MT Sykes (2000) Reply: Do low CO2 concentrations affect pollen-based reconstruction of LGM climate? Quaternary Research 53 (in press).

VI. SA Cowling, MA Maslin and MT Sykes (1999) A theory of allopatric speciation derived from palaeovegetation simulations of Amazonia. Quaternary Research (accepted, in revision).

VII. SA Cowling (2000) Carbon stress, evolutionary innovation and extinction in land plants, submitted, Global Change Biology.

VIII. SA Cowling (1999b) Plants and temperature-CO2 uncoupling. Science 285, 1500-1501.

IX. SA Cowling (2000) Rubisco adaptations to Pleistocene climate cycles. Manuscript in revision.

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