Atmosphere, ecology and evolution: what drove the Miocene expansion of C 4 grasslands?
2007; Wiley; Volume: 96; Issue: 1 Linguagem: Inglês
10.1111/j.1365-2745.2007.01323.x
ISSN1365-2745
Autores Tópico(s)Ecology and Vegetation Dynamics Studies
ResumoJournal of EcologyVolume 96, Issue 1 p. 35-45 Open Access Atmosphere, ecology and evolution: what drove the Miocene expansion of C4 grasslands? Colin P. Osborne, Corresponding Author Colin P. Osborne *Correspondence author. E-mail: c.p.osborne@sheffield.ac.ukSearch for more papers by this author Colin P. Osborne, Corresponding Author Colin P. Osborne *Correspondence author. E-mail: c.p.osborne@sheffield.ac.ukSearch for more papers by this author First published: 23 November 2007 https://doi.org/10.1111/j.1365-2745.2007.01323.xCitations: 54 Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation. AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat Summary 1 Grasses using the C4 photosynthetic pathway dominate today's savanna ecosystems and account for ~20% of terrestrial carbon fixation. However, this dominant status was reached only recently, during a period of C4 grassland expansion in the Late Miocene and Early Pliocene (4–8 Myr ago). Declining atmospheric CO2 has long been considered the key driver of this event, but new geological evidence casts doubt on the idea, forcing a reconsideration of the environmental cues for C4 plant success. 2 Here, I evaluate the current hypotheses and debate in this field, beginning with a discussion of the role of CO2 in the evolutionary origins, rather than expansion, of C4 grasses. Atmospheric CO2 starvation is a plausible selection agent for the C4 pathway, but a time gap of around 10 Myr remains between major decreases in CO2 during the Oligocene, and the earliest current evidence of C4 plants. 3 An emerging ecological perspective explains the Miocene expansion of C4 grasslands via changes in climatic seasonality and the occurrence of fire. However, the climatic drivers of this event are debated and may vary among geographical regions. 4 Uncertainty in these areas could be reduced significantly by new directions in ecological research, especially the discovery that grass species richness along rainfall gradients shows contrasting patterns in different C4 clades. By re-evaluating a published data set, I show that increasing seasonality of rainfall is linked to changes in the relative abundance of the major C4 grass clades Paniceae and Andropogoneae. I propose that the explicit inclusion of these ecological patterns would significantly strengthen climate change hypotheses of Miocene C4 grassland expansion. Critically, they allow a new series of testable predictions to be made about the fossil record. 5 Synthesis. This paper offers a novel framework for integrating modern ecological patterns into theories about the geological history of C4 plants. Carbon dioxide and the expansion of C4 grasslands Major contrasts in the climatic preferences of grass subfamilies have been noted for more than half a century (Hartley 1950), but their significance was only recognized following the discovery of C4 photosynthesis. Tropical and subtropical grasslands are dominated by the predominantly C4 Panicoideae and Chloridoideae (Hartley 1958a,b; Hartley & Slater 1960), which together account for more than half of the world's grass species (Fig. 1; Linder & Rudall 2005) and ~20% of gross terrestrial carbon fixation (Lloyd & Farquhar 1994). Their carbon-concentrating mechanism suppresses the energetically wasteful process of photorespiration that plagues C3 grasses at high temperatures, and significantly raises the efficiency of photosynthesis in warm climate regions. In contrast, C3 grass subfamilies such as the Pooideae are largely confined to temperate climates, where photorespiration is naturally limited by lower temperatures (Hartley 1961, 1973). Figure 1Open in figure viewerPowerPoint Cladogram displaying the hypothesized relationships among subfamilies of the Poaceae based on multiple markers, with the number of species shown for each, and filled circles () indicating the unequivocal origins of C4 photosynthesis in independent clades (Watson & Dallwitz 1992; GPWG 2001; Linder & Rudall 2005; Sánchez-Ken et al. 2007). Up to eight independent origination events may have occurred within the Panicoideae. The evolutionary history of these patterns was elucidated only in the past two decades, following the realization that C4 photosynthesis imparts a distinctive carbon isotope signature to plant materials and trophic pathways. By analysing the isotopic composition of fossilized soils (palaeosols) and the teeth of herbivores, geochemists uncovered a surprise; the domination of low-latitude ecosystems by C4 grasses is a recent phenomenon in geological terms, occurring only 4–8 Myr ago (Ma) at the Miocene–Pliocene boundary, when C4 grasslands expanded across at least four continents (Fig. 2; Quade et al. 1989; Cerling et al. 1997). The factors behind this evolutionary phenomenon have remained controversial since its discovery. Figure 2Open in figure viewerPowerPoint Examples of the shifts in stable carbon isotope ratio (δ13C) characterizing the Miocene rise of C4 plants in (a) Pakistan (Quade & Cerling 1995), (b) the Great Plains (Fox & Koch 2003) and (c) East Africa (Cerling et al. 1997). Values for (a) and (b) were obtained from palaeosol carbonates, and the proportion of biomass contributed by C4 plants calculated following Fox & Koch (2003). Values for (c) are from the tooth enamel of mammalian herbivores, with the proportion of C4 plants in their diets after Cerling et al. (1997). At first, debate focused on the relative merits of CO2 as a driver of C4 grassland expansion (e.g. Cerling et al. 1994; Morgan et al. 1994a,b). The case for CO2 was persuasive, and based on the premise that selective and competitive advantages of C4 photosynthesis result from the energetic benefits of eliminating photorespiration at high temperatures and low atmospheric CO2 (Ehleringer et al. 1991, 1997; Cerling et al. 1997). These advantages over the ancestral C3 condition are reversed when photorespiration is naturally suppressed by low temperatures or high CO2, because the C4 carbon-concentrating mechanism requires energy. This leads to critical thresholds of temperature (around 20–25 °C at today's atmospheric CO2 concentration) and CO2 (around 500 p.p.m. in tropical environments) where C3 and C4 photosynthesis have equal energy requirements and, by extension, equal competitive and selective advantages (Cerling et al. 1997). The proponents of this elegant hypothesis noted the close correspondence between the theoretical temperature threshold and mean growing season value in modern regions of equal C3 and C4 grass species richness, and postulated that declining CO2 crossed an equivalent threshold at the Miocene–Pliocene boundary (Ehleringer et al. 1991, 1997; Cerling et al. 1997). Their ideas were supported by a geochemical model of atmospheric CO2, which indicated the necessary decline during the Cenozoic (Berner 1998). By the late 1990s, the ideas underpinning the CO2 starvation hypothesis were widely accepted, but still awaited the crucial test provided by palaeo-CO2 reconstructions. This soon came with the publication of three data sets (Pagani et al. 1999; Pearson & Palmer 2000; Royer et al. 2001), each using an independent proxy for CO2, and each showing a long period of stasis in the level of atmospheric CO2 during the expansion of C4 grasslands (Fig. 3b; reviewed by Royer 2006). Unless these palaeo-CO2 proxy records are challenged on technical or theoretical grounds, the geological evidence therefore stands firmly against the CO2 starvation hypothesis for C4 grassland expansion, and new mechanisms must be sought. Instead, the latest evidence suggests that atmospheric CO2 dropped sharply through the C3–C4'crossover threshold' at 25–30 Ma during the Oligocene, when it initiated our modern 'icehouse' era of advancing and retreating polar ice sheets (Fig. 3; Pagani et al. 2005; Royer 2006). The emerging picture of palaeoenvironmental change therefore lends credence to an alternative hypothesis, proposing declining CO2 concentration as a key selection pressure for the evolutionary origins of C4 photosynthesis in the grasses, rather than C4 grassland expansion (Ehleringer et al. 1991; Pagani et al. 2005). Figure 3Open in figure viewerPowerPoint CO2 and climate change from the Oligocene to the present day. (a) Oxygen isotope values of deep-sea foraminifera (δ18O) displayed as a locally weighted running mean calculated by Zachos et al. (2001). This serves as a combined proxy for the global deep-sea temperature and continental ice volume, with increases in δ18O indicating cooling and ice growth. Periods of rapid ice sheet growth are indicated by 'up' arrows, and contraction by 'down' arrows. The geological timescale shows ages in Myr ago (Ma); Plio, Pliocene; Plt, Pleistocene. (b) CO2 proxy data based on carbon isotope ratios of marine phytoplankton, stomatal densities of fossil leaves and the boron isotope ratios of planktonic foraminifera compiled by Royer (2006). Palaeosol proxy data are not shown, because the uncertainty in this technique (± 500 p.p.m.) precludes meaningful estimation of low CO2 levels. Here, I review two major issues currently facing geologists, physiological ecologists and ecosystem scientists with interests in this field. I first evaluate the proposed role of CO2 in the evolutionary origins of C4 photosynthesis, focusing on the question of when the pathway first arose in the grasses. However, my principal focus is on the current debate surrounding the causes of C4 grassland expansion, particularly the hypothesized effects of climate change and fire. I argue that a deeper understanding of these proposed abiotic drivers could be achieved by explicitly considering their contrasting interactions within independent groups of C4 grasses. Dating the origins of C4 photosynthesis A crucial test of the CO2 hypothesis for C4 grass origins is to establish whether the first appearance of the pathway coincides with the Oligocene drop in atmospheric CO2. Using a molecular clock, Gaut & Doebley (1997) calculated that divergence of two major C4 grass tribes, the Paniceae and Andropogoneae (Fig. 1), occurred 25–32 Ma, leading later authors to argue that origins of C4 photosynthesis must therefore be at least this old (e.g. Kellogg 1999). However, subsequent phylogenetic analysis cast doubt on this idea, suggesting that C4 origins may have post-dated the divergence event, evolving in up to eight independent subgroups of the Paniceae and Andropogoneae (Giussani et al. 2001; Aliscioni et al. 2003; Sage 2004). Dating the nodes of the grass phylogenetic tree (Fig. 1) has proved difficult because it is becoming increasingly clear that variation in the mutation rate among branches generates large errors in molecular clocks (Pulquiéro & Nichols 2007). Attempts at calibration using the fossil record have yielded dates that vary hugely because of the low sample sizes used (Linder & Rudall 2005). More precise dating of evolutionary events within the grass family therefore depends crucially on a better resolved fossil record. Fossils only provide minimum dates for nodes of the phylogenetic tree because the geological record is incomplete. This problem is particularly acute for grasses of open habitats, where the potential for fossilization is extremely low (Cerling 1999). The oldest C4 grass macrofossils date to only 12.5 Ma in the Middle Miocene (reviewed by Osborne & Beerling 2006). However, the pollen record for grasses overall stretches back more than 65 Myr to the Late Cretaceous (Jacobs et al. 1999), indicating the potential for much earlier C4 origins. Grass pollen cannot be identified below the family level, but phytolith traits map onto the grass phylogeny at the subfamilial scale (Piperno & Sues 2005; Prasad et al. 2005). Phytoliths form, to a varying degree, in all groups of living vascular plants (Piperno 2006). However, grasses have a higher silica production than most other plants (Hodson et al. 2005), and phytoliths in this family are more diagnostic than for most other plant groups. The interpretation of fossil phytolith assemblages is complicated by multiplicity (each species produces more than one phytolith morphotype), and redundancy (different species produce similar morphotypes) (Piperno 1988). Nevertheless, the comparison of fossil assemblages with modern reference collections has allowed robust statistical inferences about the phylogenetic affinities and ecology of extinct grass communities (Strömberg 2004, 2005). Phytolith analysis has been used to identify grasses with affinities to the PACCMAD crown group (Fig. 1) from 65- to 67-Myr-old dinosaur dung in India (Prasad et al. 2005), and from the predominantly C4 subfamily Chloridoideae (Fig. 1) in 19-Myr-old Great Plains sediments (Strömberg 2005). Although this technique cannot establish when C4 photosynthesis originated in each clade, complementary methods have been developed for analysing the carbon isotopic signature of phytolith assemblages (Smith & White 2004). Interpretation of these data is difficult because of interspecific variation and differences in the biochemical nature of carbon compounds between C3 and C4 grass phytoliths (reviewed by Smith & White 2004). However, preliminary data suggest that up to 50% of Great Plains grasses may have used the C4 pathway by 12 Ma (Smith 2001). Geochemical analyses of herbivore teeth, palaeosols and the molecular markers of plant cuticles trace the C4 carbon isotope signal back to 16–18 Ma in the Early Miocene (reviewed in Tipple & Pagani 2007). These data are consistent with the presence of C4 grasses comprising up to 30% of the total biomass in tropical and subtropical ecosystems throughout the Miocene (Fox & Koch 2003; Pagani et al. 2005; Tipple & Pagani 2007). However, the use of bulk isotope analyses to estimate C4 biomass in extinct plant communities is not a precise science. Critical uncertainties remain about the isotopic composition of atmospheric CO2 through geological time, variation in the background signal caused by the water relationships of C3 plants and the taxonomic identity of the C4 plants (Tipple & Pagani 2007). Partial resolution of these issues may come from a new analytical technique for measuring the carbon isotope composition of tiny samples, which currently allows C3 or C4 pathways to be identified from individual pollen grains with > 85% reliability (Nelson et al. 2007). This emerging method should enable researchers to establish directly the photosynthetic pathway of parent plants using grass pollen recovered from sediments dating to the Early Miocene and Oligocene. Unlike analyses of palaeosol or tooth carbon, this technique does not require abundant C4 plant biomass to resolve a C4 signal from the C3 background and offers the potential for identifying rare C4 plants in a predominantly C3 community, in addition to allowing identification of taxa to at least the family level. Furthermore, because it contrasts 'pure C3' with 'pure C4' samples, the technique is not compromised by variations in the isotopic signature of atmospheric CO2. Pollen-based evidence may therefore bridge the gap between postulated C4 origins and our oldest current evidence for C4 plants. However, questions will still remain over the precise taxonomic identity of these plants, and pinning down the earliest C4 grasses is only part of the challenge confronting geologists in this field. Plummeting CO2 concentrations were correlated with a whole suite of climatic changes during the Oligocene, including falling temperature and increasing aridity (Fig. 3; Zachos et al. 2001; Dupont-Nivet et al. 2007), and may not have been the only selection pressure for C4 photosynthesis. Hypothesized drivers of C4 grassland expansion Geological evidence therefore raises two linked questions. If CO2 was not the driving force, what caused the Miocene–Pliocene expansion of C4 grasslands? And, if C4 grasses were present from the Early Miocene onwards, why did they not dominate ecosystems earlier in their evolutionary history? The key to answering both of these questions may lie in fossil evidence that documents an abundance of woody C3 plants throughout the Miocene, forming forests, woodlands or savannas in regions that subsequently became C4 grasslands (reviewed by Osborne & Beerling 2006). Woody plant cover exerts a major limitation on C4 grass abundance, because trees and shrubs rapidly overtop herbaceous plants in the absence of disturbance, and most C4 species are intolerant of shading (Sage et al. 1999; Sage & Pearcy 2000). Explanations of C4 grassland expansion in the geological record therefore evoke a combination of climatic and disturbance factors that reduce tree cover, focusing primarily on changes in rainfall patterns and fire regime. A number of alternative palaeoclimate hypotheses have been developed. The first is supported by the oxygen isotope signature of palaeosols in South Asia, and proposes that the Miocene replacement of C3 woody vegetation by C4 grasslands was driven by a strong increase in rainfall seasonality, caused by abrupt intensification of monsoon systems (Table 1; reviewed by Osborne & Beerling 2006). A second hypothesis based on oxygen isotope data from freshwater bivalve shells in Nepal suggests a decrease in the total amount of rainfall with no significant change in seasonality (Dettman et al. 2001), and a similar mechanism is evoked for East Africa, rooted in model simulations for the region (Table 1; Sepulchre et al. 2006). Both of these climatic drying hypotheses propose that an increased frequency and intensity of drought events killed trees and allowed the incursion of C4 grasses, to produce more open savanna or grassland vegetation (Table 1). Both are linked ultimately to tectonic events, including episodes of mountain building such as the uplift of the Tibetan Plateau and East African Rift system, or changes in ocean circulation triggered, for example, by closure of the seaway between the Americas (reviewed by Osborne & Beerling 2006). Table 1. Comparison of the key hypotheses evoked to explain the Miocene–Pliocene expansion of C4 grasslands. Alternative hypotheses are not mutually exclusive, and overlap to a significant extent. For example, a change in the fire climate could also be the ultimate reason for an ecotone shift (Keeley & Rundel 2003, 2005). Hypothesis Climatic seasonality Climatic drying Ecotone shift Fire climate change Ultimate reason for Miocene–Pliocene C4 grassland expansion Development of seasonal climates with hot wet season and a dry season Decrease in total rainfall without significant shifts in seasonality C4 grasses evolved characteristics that allow displacement of woody plants from mesic habitats Development of seasonal climates promoted fires Mechanism of C4 grassland expansion Woody plant mortality during annual dry season Intensified drought events increased woody plant mortality Shift in the C4 grass– woody plant ecotone to wetter (mesic) habitats Increased frequency of fire prevented woody plant establishment Why did C4 grasses not dominate ecosystems earlier in the Miocene? Aseasonal climates favoured woody species Wet climates favoured woody species C4 grasses had not yet evolved characters allowing domination of mesic habitats Infrequent fires allowed establishment of woody plant communities Region South Asia South Asia, Africa South Asia, Africa, North America South Asia, China, West Africa Key evidence Palaeosol 18O ratios Freshwater bivalve 18O ratios (rainfall seasonality) Palaeosol structure Charcoal records Monsoon indicators Model simulations Analogy with modern ecosystems References Quade et al. (1989, 1995) Dettman et al. (2001), Sepulchre et al. (2006) Retallack (2001) Keeley & Rundel (2003, 2005) An alternative viewpoint has emerged from analyses of palaeosol structure, which use the soil horizon structure to infer a vegetation type of desert, grassland or woodland, and the depth of the calcic horizon to estimate rainfall amounts (Retallack 2001). Application of this approach to geological sediments suggests that spatial gradients in rainfall generated parallel regional variation in vegetation (Fig. 4). Ecosystems varied from desert grassland to dry woodland throughout the Early and Middle Miocene in South Asia, the central and western United States and East Africa (Fig. 4; reviewed by Retallack 2001). Palaeobotanical evidence from East Africa also indicates savanna and woodland vegetation during the Early and Middle Miocene (Jacobs et al. 1999). However, the inference of dry climates is not supported by plant macrofossils, phytoliths and pollen from the Great Plains, which indicate productive savanna or woodland vegetation with a significant C3 grass component (Jacobs et al. 1999; Strömberg 2004, 2005). The presence of palms, gingers and bamboos (Strömberg 2004), woody dicots confined to moister climates today (Axelrod 1985), and giant tortoises and alligators (Hutchinson 1982) suggests a relatively humid, rather than arid, climate. Palaeosol data suggest a major change in the ecology of these ecosystems during the Late Miocene, with C4 grasses displacing woodland communities in mesic regions and shifting the grassland–woodland ecotone to higher rainfall areas in North America, Africa and Asia (Table 1, Fig. 4; Retallack 2001). The causes of this ecotone shift are unknown, but have been attributed to the coevolution of grasses and grazers (Retallack 2001), and significant changes in fire regime resulting from shifts in the seasonal distribution, but not total amount, of rainfall (Keeley & Rundel 2005). Figure 4Open in figure viewerPowerPoint Precipitation estimates based on depth to the calcic horizon in palaeosols from (a) Pakistan, (b) the central USA and (c) East Africa (Retallack 2001). The grey-shaded area denotes the total range of values obtained for all palaeosol types (originating in deserts, grasslands, woodlands and forests), and the symbols show values obtained for mollic palaeosols, which develop only beneath sod-forming grasses (Retallack 2001). These data suggest that grasslands invaded wetter areas from 8 Myr ago (Ma). Evidence supporting a linkage between fire and the expansion of C4 grasslands comes from black carbon (BC) abundance in marine sediments, a geological proxy for fire occurrence. BC increases by 100- to 1000-fold in Pacific Ocean localities downwind of the Indian subcontinent (Herring 1985; Keeley & Rundel 2003), and 5-fold in the South China Sea (Jia et al. 2003), during the Miocene–Pliocene interval of major C4 grassland expansion in these regions. Sediments off the Atlantic coast of West Africa also show significant increases in charred grass cuticle and pollen abundance during the same period (Morley & Richards 1993). In the last 5 years, a new and compelling hypothesis has therefore added ecosystem-scale feedbacks between fire and vegetation to previous ideas about palaeoclimate (Table 1; Keeley & Rundel 2003, 2005). Fire sustains C4 grasslands by killing woody plants and entrains a positive feedback because the dead foliage of grasses provides abundant fuel for fires, thereby increasing tree mortality and promoting the further spread of grasses (Keeley & Rundel 2003, 2005). The fire hypothesis therefore proposes that increasing climatic seasonality during the Late Miocene raised fire frequency by supporting rapid biomass production and the development of a high fuel load during wet summer conditions. Intensifying winter drought promoted drying, and increased the likelihood that this material would ignite, with ignition itself provided by lightening strikes at the end of the dry season. Further feedbacks on the fire regime have been proposed via the hydrological cycle (Beerling & Osborne 2006) and wind strength (Tipple & Pagani 2007), but these remain speculative at present. Ecosystem fire regimes show an important interaction with climate. Fuel remains too moist to support frequent fires in wet, aseasonal environments, whilst the low productivity of dry climate regions produces too little fuel to carry significant fires (Keeley & Rundel 2005). However, given sufficient periods of dry weather, fire has the potential to displace mesic forests in favour of grasslands. This is demonstrated in modern ecosystems by complementary data from: model simulations showing that fire reduces forest cover by ~50% at the global scale (Bond et al. 2005); analysis of woody plant cover across Africa indicating that significant areas of savanna are maintained by disturbance in regions with sufficient rainfall to support forest (Sankaran et al. 2005); fire exclusion experiments which allow the establishment of fire-sensitive trees in mesic savanna ecosystems (Bond et al. 2003, 2005); and the fire-mediated replacement of native forests on Pacific Islands by invasive grasses (D'Antonio & Vitousek 1992). These observations each provide indirect support for the hypothesized mechanism of vegetation change at the Miocene–Pliocene boundary. An emerging consensus therefore evokes interactions between palaeoclimate change, vegetation–climate relationships and fire frequency to explain the Miocene expansion of C4 grasslands (Table 1; Keeley & Rundel 2005). This 'consensus scenario' suggests that Early and Middle Miocene landscapes were dominated by C3 forests or woodlands, with C4 grasses occupying open ground between the patches of woody plants. Increasing seasonality during the Late Miocene concentrated rainfall into a hot growing season, creating a fire regime that removed woody vegetation and shifted the woodland–grassland ecotone to wetter areas (Table 1). Formulated in this way, the hypothesis asserts that climates capable of supporting frequently burning mesic C4 grasslands at the expense of woodland and forests were absent during the Early and Middle Miocene. However, application of the hypothesis to North and South America is problematic in two important respects. First, patterns of climatic change in these regions at the Miocene–Pliocene boundary are less clear than those in Asia, and an increase in rainfall seasonality has yet to be demonstrated (Passey et al. 2002; Fox & Koch 2004; Osborne & Beerling 2006). Secondly, pollen records, phytolith assemblages and mammalian tooth morphology suggest that a transition from closed forest to open woody vegetation with a significant C3 grass component may have occurred as early as 25 Ma (Late Oligocene to Early Miocene) in the Great Plains (Strömberg 2004, 2005) and 32 Ma (Early Oligocene) in South America (Jacobs et al. 1999). The adaptive radiation of specialist grazers (Strömberg 2006) and an extremely high browser diversity in these Great Plains ecosystems resulted in species-rich mammalian herbivore communities by 15 Ma (Janis et al. 2000). Carbon isotope data demonstrate that some grazers showed a dietary shift in the Late Miocene, subsisting almost exclusively on C4 plants for the 2 Myr before C4 grassland expansion, with presumably significant, but currently unknown, effects on grass–tree dynamics (Fox & Koch 2004; Beerling & Osborne 2006). I argue that our overall understanding and ability to test climatic and ecological hypotheses regarding Miocene ecosystems would be improved by an explicit consideration of C4 grass phylogeny. To make this case, I first present biogeographical data indicating significant contrasts in the abundance of different C4 grass clades along rainfall gradients, and show how this information might be used in hypothesis testing. Secondly, I re-analyse a published data set in the same context, suggesting that changes in the species richness of independent C4 grass lineages track the length of the rainy season. Finally, I present intriguing preliminary evidence of fire controls on the abundance of particular C4 clades. Contrasting climate relationships of C4 grass clades The subfamilies Panicoideae and Chloridoideae together account for the majority of modern C4 grass species (Fig. 1; Linder & Rudall 2005), but analyses of regional biodiversity patterns suggest a crucial difference in the climate relationships of these major clades. For the United States and Argentina, the percentage of C4 species belonging to the Panicoideae shows a positive correlation with annual rainfall, whereas the same relationship for the Chloridoideae is negative (Fig. 5; Taub 2000; Cabido et al. 2007). Figure 5Open in figure viewerPowerPoint (a) Percentage of C4 grasses in US floras belonging to the Panicoideae () and the Chloridoideae ○) subfamilies (Taub 2000). (b) Percentage of C4 grasses in floras with the NADP-ME () and NAD-ME (○) subtypes in the USA (Taub 2000) and (c) Australia (Hattersley 1992). Because each flora covers a differing geographical area, values are expressed as a percentage to normalize for species–area biases. (a) and (b) express the same data set on a different basis, excluding (a) members of the Aristidoideae, and (b) species with the PCK subtype of C4 photosynthesis. The mechanisms underpinning these relationships are unclear at present, but may be linked to the close association between biochemical subtypes of C4 photosynthesis and specific phylogenetic groups; the majority of Panicoideae species utilize the NADP-malic enzyme (NADP-ME) pathway whereas most members of th
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