Apparent changes in the Ordovician–Mississippian plant diversity

Review of Palaeobotany and Palynology 227 (2016) 19–27

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Apparent changes in the Ordovician–Mississippian plant diversity Borja Cascales-Miñana 1 CNRS, UMR Botanique et Bioinformatique de l'Architecture des Plantes (AMAP), Université Montpellier 2, Montpellier F-34000, France

a r t i c l e

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Article history: Received 13 May 2015 Received in revised form 11 October 2015 Accepted 23 October 2015 Available online 31 October 2015 Keywords: Eoembryophytic phase Euphyllophytes Lycophytes Plant megafossil Spore diversity Terrestrialization

a b s t r a c t This study aims to approximate an illustrative vision of the apparent temporal dynamics of land plant diversity during the terrestrialization process (i.e., the invasion of the land by plants). This problem has often been addressed through studying the Silurian–Devonian megafossil-based diversity patterns of land plants (embryophytes). However, the inclusion of the dispersed spore fossil record is essential for characterizing the first steps of this process (i.e., Eoembryophytic flora). Consequently, this new study includes both spore taxa and plant megafossils in order to discern the diversity trajectories from the first phases of early land plant diversification until the stabilization of early Carboniferous forests (i.e., Palaeophytic flora). The diversity patterns of the primary recognized plant lineages (i.e., Lycophyta and Euphyllophyta) have been also traced in order to discern the origin of the major fluctuations of plant megafossil-based diversity. Results reveal that while the dispersed spore diversity curve shows a sustained increase towards the end of the Devonian Period – with a first maximum towards the late Silurian – the megafossil embryophyte diversity curve is characterized by a set of sequential ascending peaks at the Pragian (Early Devonian), Givetian (Mid-Devonian), and Visean (Mississippian), with a single significant depletion in the Eifelian (Mid-Devonian). The comparative analysis of the lycophyte and euphyllophyte diversity patterns suggests that the substantial embryophytic diversity changes are driven by diversification within lineages rather than by the rhythm of the appearance of key morphological traits. This evidence (1) advocates for an intrinsic ecological control on the apparent changes in taxic richness and (2) implies that the observed plant diversity dynamics respond to the overlapping of the various expansion phases of the plant lineages involved. © 2015 Elsevier B.V. All rights reserved.

1. Introduction This paper attempts to highlight the temporal pattern of terrestrial plant diversity during the terrestrialization process (i.e., the invasion of the land by plants, Vecoli et al., 2010). Plants were central to the conquest of land by life. Plants are primary producers, the base of trophic chains, as well as the key element leading to soil formation. Understanding early plant diversity dynamics is therefore critical in advancing towards a holistic view of the terrestrial biosphere. The study of the dynamics of continental environments' colonization by land plants (embryophytes) has been traditionally addressed using the Silurian–Devonian megafossil-based diversity patterns (i.e., by using fossils representing a significant portion of the plant, Wellman, 2010). The best example of this approach is the pioneering work performed by Niklas et al. (1985, Fig. 1). This work illustrates the specieslevel diversity curve of plant diversity from the Late Silurian to the Famennian by disentangling the major diversity changes of different plant groups. From this, a sustained increase in diversity can be observed until the latter part of the Mid-Devonian, along with a drop in E-mail addresses: [email protected], [email protected]. Present address: PPP, Département de Géologie, Université de Liège, Allée du 6 Août, B18 Sart Tilman, B4000 Liège, Belgium. 1

http://dx.doi.org/10.1016/j.revpalbo.2015.10.005 0034-6667/© 2015 Elsevier B.V. All rights reserved.

diversity towards the Carboniferous. This and other of Niklas's works (see, e.g., Niklas, 1988; Niklas and Tiffney, 1994; Niklas et al., 1980, 1983) are iconic and still represent the current paradigm in the study of diversity in early plants. Other researchers have also attempted to reconstruct the diversity patterns of early land plants through the use of megafossil data, but using restricted time intervals (see, e.g., Chaloner and Sheerin, 1979; Richardson and Edwards, 1989; Edwards, 1990; Raymond et al., 2006; Morris and Edwards, 2014) or concrete plant groups (see, e.g., Cascales-Miñana and Meyer-Berthaud, 2015; Meyer-Berthaud et al., 2010) rather than providing (as in Niklas's studies) an integrated view of the expansion of early floras. Of special relevance are recent studies performed using the South China plant fossil record. Thus, for instance, Xiong et al. (2013, Fig. 1) described sequential episodes in the diversification of Silurian–Mississippian land plants characterized by four diversity peaks (Pragian, Givetian, Famennian, and Visean) rather than a sustained increase in diversity. This latter view implies a change in comparison with the classic conception of the diversification of early land plants, although these results cannot yet be extrapolated to a worldwide scale. The first unequivocal megafossil evidence of embryophytes is registered in the Homerian (Late Wenlock) ca. 428 Ma (i.e., Cooksonia, Edwards et al., 1983). However, the oldest evidence of plants predates the Homerian stage by more than 50 Myr (Edwards and Wellman,

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2001). Rubinstein et al. (2010) reported the earliest unequivocal embryophyte traces (i.e., cryptospores) from the Dapingian (early Middle-Ordovician, 470–467 Ma). This scenario implies that (1) the megafossil embryophyte fossil record only allows a partial view of the early colonization of land ecosystems and (2) that including the microfossil-based plant diversity patterns is therefore essential in characterizing the first steps of this process (i.e., Eoembryophytic phase sensu Gray, 1993). Several studies have either performed spore diversity counts for the Ordovician–Silurian time interval (see, e.g., Steemans, 1999, 2000; Steemans and Wellman, 2004; Wellman et al., 2013) or focused on discussion of the earliest diversity trends of the dispersed spore fossil (also known as microfossil) record (see, e.g., Edwards et al., 2014; Gray, 1985; Kenrick et al., 2012; Steemans et al., 2012; Wellman and Gray, 2000; Wellman et al., 2003) as way to characterize the origin and subsequent diversification of an incipient terrestrial biota. In 1993, Gray recognized three key phases within the Paleozoic land plant diversification. The first phase (the so-called Eoembryophytic, Mid-Ordovician to Late Llandovery, ca. 470–435 Ma) corresponds to a bryophyte-like flora. This phase is only captured in the dispersed spore fossil record. The second, or Eotracheophytic, phase (Late Llandovery to Mid-Lochkovian, ca. 435–415 Ma) corresponds to the radiation of the earliest vascular plants (tracheophytes), while the last, Eutracheophytic, phase (Late Lochkovian to Mid-Permian, ca. 412– 260 Ma) corresponds to major diversification events of tracheophytes, e.g., the origin and diversification of seed plants (Gray, 1993; Kenrick and Crane, 1997b; Le Hir et al., 2011). More recently, it has been suggested that in terms of ecological (and evolutionary) replacement, Gray's (1993) final two phases more accurately embrace the rise of the three different dynamics (Rhyniophytic, Eophytic, and Palaeophytic floras). These are represented by the very earliest tracheophytes (Mid-Silurian and Early Devonian), the homosporous plants, e.g., Zosterophylls and early lycopsids (Early and Mid-Devonian), and the Late Devonian and Carboniferous flora characterized by the dominance of the heterosporous plants and the early gymnosperms (i.e., seed ferns), respectively (Cleal and Cascales-Miñana, 2014). The Ordovician–Mississippian time interval therefore spans the conquest of land by the earliest plants (i.e., Eoembryophytic flora sensu Gray, 1993) until the stabilization of the Carboniferous tropical wetlands and early forests, which were largely dominated by heterosporous free-sporing plants and early gymnosperms (i.e., Palaeophytic flora sensu Cleal and Cascales-Miñana, 2014). In addition, in a recent study, Xue et al. (2015) have shown how the Devonian–Mississippian time interval, which is characterized by a great increase of plant diversity driven by a rise in the morphological disparity of leaves, is essential to our understanding of the configuration of early land ecosystems. The analysis presented in this paper differs from previous studies in that it (1) integrates the plant diversity dynamics from the first phases of early land plant diversification processes until the development of a complex vegetation, (2) considers both spore taxa and plant megafossil remains to discern the diversity trajectories of the Eoembryophytic– Palaeophytic transition, and (3) disentangles the diversity patterns of the main recognized plant lineages as well as the relationship dynamics and balance between the plant groups involved. In this way, this new analysis aims to help increase our collective understanding of the observed temporal distribution of the first vegetation changes recovered in the known fossil record. 2. Data A new compilation of plant fossil data for the Ordovician– Mississippian time interval was prepared. Mega- and microfossil evidence was considered. For each entry, the data were derived from primary literature, but secondary sources were also used to correlate with the original citation. For instance, this study reused the regional mega- and microfossil data from South China extracted by Xiong et al.

(2013) to adapt the temporal distribution of non-endemic taxa at a global scale. It also included the microfossil data compiled by Wellman et al. (2013), which covers, for example, the distribution of cryptospores from the Ordovician to the end of the Silurian Period. Likewise, it also referenced recent revision studies that provide an updated version of key fossiliferous formations and regions with a large recognized diversity, such as the Lochkovian plant remains of the Welsh Borderland (UK, see Morris and Edwards, 2014), the plant diversity collected from the Posongchong Formation (Yunnan province, see Hao and Xue, 2013), the region of Southeastern Mountainous Altay (Southern Siberia, see Gutak et al., 2011), the Campbelton Formation (New Brunswick, see Kennedy et al., 2012), and the Late Devonian Red Hill site (Pennsylvania, see Cressler et al., 2010), among others. Both classic and more recent monographies were also referenced (e.g., Anderson et al., 2007; Cleal, 1993a,b), as well as recent compilations based on distinct Devonian plant groups (e.g., Zosterophyllopsida, Cascales-Miñana and Meyer-Berthaud, 2014, 2015) or well-documented inventories of diversity data traced at regional scale (see, e.g., Gerrienne, 1993). Together with sources of these kinds, information provided from online relational databases of diversity data (e.g., Paleobiology database) was also considered. This was done using the Fossilworks platform (http:// fossilworks.org/). During compilation, plant names were filtered using the Index Nominum Genericorum (http://botany.si.edu/ing/) to avoid redundancies and discuss affinities as well as the plant organ preserved in some cases. Raw data were originally prepared at the species-level, but initial results showed several constraints, due to which this level was avoided for the purposes of data analysis. Species diversity is constrained by (1) a significant number of synonyms, (2) a singular limitation due to the plant organ preserved (e.g., some species are based on complete foliage while others only from a pinnule), and (3) a high prevalence of endemism, which makes it difficult to measure diversity by extending any temporal range. This last constraint is especially delicate for the time interval covered in this study. In contrast, genus-level data analysis (1) tends to minimize overestimation of observed diversity, (2) facilitates the evaluation of synonyms, and (3) enables assessment of the whole stratigraphic distribution of plant diversity by diminishing single species occurrences (i.e., species that occur in a single site). Furthermore, the nomenclature of Ordovician–Mississippian plant occurrences is very rich in tentative assignations, for example, sp., aff., cf., ?. This situation generates an unclear volume of information regarding affinities and potentially inflates the observed richness. Compiled data showed that taxonomy is less biased by these kinds of inaccuracies in genus-level determinations. Thus, although this approach does not allow reporting potential within genus radiations, genus-level data analysis was nonetheless carried out in the course of this study on the basis that the morphological evolution of plants captured by the diversity of genera represents a reasonable proxy of major changes in phytodiversity through time. Analysis of land plant diversity patterns was based on the apparent diversity changes over time (i.e., diversity taken at face value, Foote, 2001). This analysis was conducted at stage-level from the MidOrdovician (Dapingian) until the end of the Mississippian (Serpukhovian); therefore, 24 time intervals were considered according to the International Stratigraphic Chart (2015, http://www.stratigraphy.org/ ICSchart/ChronostratChart2015-01.pdf). The temporal distribution of compiled genus-level diversity was manually tabulated between the first- and last-appearance data (i.e., FADs and LADs, respectively) by assuming continuous ranges between them (i.e., range-through method, Boltovskoy, 1988). Mega- and microfossil plant diversities were tabulated separately for analysis. Raw data included the temporal distribution of 740 genera, with 505 belonging to megafossil-based plant evidence. Initial results showed that this compilation provides a sufficient representativeness of diversity signal to elucidate, at least, the major changes and main trends in the diversity of early floras; however, due to the dynamic nature of fossil data, the diversity patterns exposed below may be

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subject to modifications as further data and/or different interpretations become available and/or are incorporated due to ongoing researches. Thus, the revealed diversity dynamics, particularly the spore diversity patterns, must be taken only as a first approach of problematics. Raw charts of megafossil plant and dispersed spore diversity data can be found in Data S1. 3. Methods Three different metrics were used to estimate the changes in the diversity of embryophytes through the Ordovician–Mississippian time interval. First, diversity patterns were extended based on the total observed diversity per time unit. This measure is a classic approach to diversity studies through time and provides an intuitive idea of the major fluctuations of known diversity across a given time interval. However, when diversity is represented based on a system of time intervals, this can generate overestimation of the temporal distribution of some taxa, For instance, this applies in the case of Serrulacaulis, which ranges from the Eifelian (Mid-Devonian) to the early Frasnian (Late Devonian) (Berry and Fairon-Demaret, 2002; Hueber and Banks, 1979; Lessuise and Fairon-Demaret, 1980). The same also occurs for some single-interval taxa, e.g., Wuxia (Berry et al., 2003) or Rotafolia (Wang et al., 2005) documented from the late Famennian (Late Devonian). Due to this, an analysis of the fluctuations of mean standing diversity was also performed in order to minimize such effects for comparison. For a given time interval, total diversity does not infer the actual diversity in any moment during that time interval. This is because we cannot be confident about that the entire spectrum of FADs occurs before the LADs (Bambach et al., 2004). The only way to be sure of the actual diversity at any one point is by focusing the diversity estimation at the interval boundaries. The standing diversity responds to this principle. Thus, the mean standing diversity is obtained by halving the sum of the top boundary crossers (i.e., the standing diversity at the boundary between the interval and its succeeding interval) and the bottom boundary crossers (i.e., the standing diversity at the boundary between the studied interval and its preceding interval). Alternatively, the standing diversity can be also calculated by subtracting half of FADs and LADs from the total diversity (Foote, 2000). This diversity estimate thereby captures solid diversity trends by avoiding the computation of singleinterval taxa (so-called singletons, Fitzgerald and Carlson, 2006). Bambach et al. (2004) emphasized, however, that changes in diversity are best illustrated by comparing diversity at the start of different intervals. Thus, as a third measure, the boundary-crossing standing diversity (i.e., the initial diversity of the considered interval) was also plotted (Alroy, 2008). This last metric has the advantage of illustrating the general trajectory of the turnover processes (i.e., the FAD-LAD balance) within intervals (Bambach et al., 2004), and – similarly to the mean standing diversity – avoids the use of singletons to estimate the diversity per time interval, which can inflate the diversity pattern from time intervals with fossil sites of an exceptional, or rare, preserved diversity (i.e., Lagerstätten effect; see Alroy, 2010). For interpretation, positive trends of boundary-crossing standard diversity indicate that the number of taxa entering in the considered interval i, from the previous interval i − 1, is greater than that the number of taxa entering in i − 1; or in other words, the volume of FADs exceeds the LADs. Conversely, negative trends indicate that the volume of LADs exceeds the FADs, following the same reasoning. Two rounds of analysis were performed. In the first round, the megafossil-based plant diversity curves were compared with the microfossil-based patterns. Following this, in order to detect major palaeofloristic changes, a second round was conducted using the Silurian–Mississippian plant megafossil diversity. The intention of this was to develop the diversity trajectories of monophyletic lineages. To this end, the diversity patterns of lycophytes (i.e., zosterophylls, drepanophycales, lycopodiales, isoetales, selaginellales, proto, and

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lepidodendrales, Kenrick and Crane, 1997a) and euphyllophytes (i.e., trimerophytes, monilophytes, and lignophytes, Crane et al., 2004; Gerrienne et al., 2010; Tomescu, 2009) were compared. Furthermore, to gain a deeper understanding of these dynamics, the analysis also traced the trajectories of lycopsids (Kenrick and Crane, 1997a) and lignophyte (i.e., progymnosperms and spermatophytes, Gerrienne et al., 2010; Meyer-Berthaud et al., 2010) diversity. From this, it was possible to characterize changes in dominance (i.e., turnover events) of major groups within early floras.

4. Results Fig. 1 depicts the megafossil-based diversity curve of embryophytes during the Silurian–Mississippian time interval. Overall, megafossil plant diversity follows an ascending trajectory from the Silurian to the end of the Mississippian Epoch. There are particularities, however. The total diversity registers three maximums at the Pragian (Early Devonian), Givetian (Mid-Devonian), and Visean (Mississippian) stages. Two important pulses of diversity are also detected at the Lochkovian (Early Devonian) and the Famennian (Late Devonian) (Fig. 1A). However, the standing diversity pattern shows that such heydays have a significant influence on single-interval records (Fig. 1B), which respond to contributions of endemic morphologies (e.g., the Pragian flora of South China) or isolated records of plant organs (e.g., Xenotheca). The boundary-crossing diversity trajectory (Fig. 1C) confirms this observation but also reveals a key diversity depletion in the Eifelian (Mid-Devonian), which represent a unique and significant loss of diversity in the global pattern. Fig. 1C highlights, in addition, a positive diversity trend during the Early Devonian; following this, only three important increments of diversity are observed in the Famennian, Visean and Serpukhovian. The Ordovician–Mississippian dispersed spore diversity curve is shown in Fig. 2. Similarly to the megafossil data, the diversity trajectory shows a general positive trend; however, the fluctuations of spore diversity over time can be interpreted into a three-phase diversification pattern. From the Mid-Ordovician to Telychian, dynamics are characterized by an initial diversity pulse followed by minor fluctuations (Fig. 2A). Following this, a second dynamic (Sheinwoodian-Pridoli) is characterized by an increase in diversity, registering a first maximum value towards the end of Silurian (Fig. 2A). We then see a final positive trend of microfossil-based diversity, which reflects an important pulse at the Emsian (Early Devonian) and a sustained growth until the Famennian, where the maximum diversity is registered (Fig. 2A). This diversity trajectory is supported by the standing diversity (Fig. 2B) and by the boundary-crossing pattern (Fig. 2C). The boundary-crossing pattern shows, in addition, a smooth depletion of diversity between the Ludfordian and the Pragian (Fig. 1C). Then again, results suggest that the general megafossil-based plant diversity pattern is triggered by the overlapping of different diversity dynamics. The comparative analysis of the diversity trajectories of major plant lineages (Fig. 3) shows, for example, that the Pragian and Givetian diversity peaks have different origins: while the first is driven by lycophytes, the second responds to euphyllophyte diversity changes (Fig. 3A). Interestingly, Fig. 3A also shows that these peaks do not correspond to increases in either lycopsids or lignophytes. Thus, this scenario implies that zosterophylls in the Pragian (Cascales-Miñana and MeyerBerthaud, 2015) and monilophytes in the Givetian (probably cladoxylopsids, see Meyer-Berthaud et al., 2010), triggered this dynamic. Furthermore, we see that despite the fact that that the standing diversity curves of lycophytes and euphyllophytes (Fig. 3B and C) show trajectories characterized by a continuous increase from the Eifelian until the Visean, there are also distinct differences. Fig. 3C shows that the lycophyte diversity registers an apparent equilibrium phase after the Famennian, while the euphyllophyte diversity continues to increase, driven by the lignophyte diversity changes.

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Fig. 1. Silurian–Mississippian genus-level megafossil-based diversity curves of land plants (embryophytes) generated from the data presented in Data S1. (A) Total observed diversity. (B) Mean standing diversity. (C) Boundary-crossing standing diversity. The diversity trajectories are scaled according to interval lengths at stage-level. White-gray boxes indicate major time intervals at epoch-level. Figure shows the apparent pattern of registered morphological diversity taken as proxy of the early plant diversity dynamics.

5. Discussion Fig. 1 plots the apparent changes in genus-level land plant diversity based on megafossil data. This diversity dynamic starts in the Homerian (Late Wenlock) according to the accepted consensus regarding the earliest plant megafossil evidence (see, e.g., Wellman, 2010, Fig. 1). There are however some pre-Homerian records of terrestrial organisms classically studied in the framework of Palaeobotany, which (despite being originally listed) have been not included in the data analysis due to their uncertain affinities, such as (for example) the nematophytes. The nematophytes (e.g., Berwynia, Lepidotruncus,

Mosellophyton, Nematophyton, and Prototaxites) are an enigmatic group of Silurian–Devonian organisms, some of which could represent remains of ancient liverworts (Graham and Gray, 2001; Graham et al., 2004), or (as in the case of Prototaxites) the remains of enormous saprophytic fungal fruiting bodies, although this affinity is disputed (Retallack and Landing, 2014). Another disputed record is Eohostimella (Gray, 1984; Strother and Lenk, 1983) from the Llandovery (Early Silurian), although recently Wellman et al. (2013, Table 29.1) have included it in their data compilation of the Silurian plant megafossil assemblages. The inclusion of this type of putative evidence (less than 3% of total sample) does not distort our perception of the plant megafossil-based

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Fig. 2. Ordovician–Mississippian genus-level dispersed spore diversity curves of land plants (embryophytes) generated from the data presented in Data S1. (A) Total observed diversity. (B) Mean standing diversity. (C) Boundary-crossing standing diversity. The diversity trajectories are scaled according to interval lengths at stage level. White-gray boxes indicate major time intervals at epoch-level. Figure shows the apparent pattern of registered morphological diversity taken as proxy of the early plant diversity dynamics.

diversity patterns; with a single exception, their inclusion would extend the diversity signal until the Katian (Late Ordovician), but only like a basal line. The plant fossil record is subdivided into plant megafossils and dispersed spores (e.g., Steemans et al., 2012; Wellman et al., 2013). The difference between them is substantial. It is well known that the plant megafossil record is much more biased than the plant microfossil record, and primarily recovers lowland palaeodiversity (see, e.g., Edwards, 1990). As noted by Wellman et al. (2013), this difference is related to the fact that spores (1) are produced in vast quantities, (2) have a high fossilization potential as consequence of the sporopollenin wall (when this sporopollenin wall is not too thin), and (3) have the capacity to be transported large distances. This is important because the longterm variations of microfossil-based diversity trends could function indirectly as a control of the general megafossil-based diversity trend during the earliest radiation of Silurian tracheophytes. For instance, more than 40 different morphologies of dispersed spores have been counted in the Gordstian (Early Ludlow), but only six plant genera

have been identified. Evidence therefore seems to suggest that the known genus-level megafossil diversity of plants underestimates the richness of Eotracheophytic flora. It is, however, during the Eoembryophytic phase of plant evolution that the apparent spore diversity changes acquire a special relevance. The Eoembryophytic spore diversity pattern (Mid-Ordovician to the end of the Telychian Stage) shows, after an initial diversity pulse in the Katian (Late Ordovician), no great variations until the Sheinwoodian (Mid-Silurian) (Fig. 2A). This pattern embraces the apparent diversity changes of obligate cryptospores and monads and non-obligate dyads (Wellman et al., 2013, Fig. 29.1). Cryptospore producers are related to basal (i.e., protracheophyte) embryophytes (see, e.g., Steemans et al., 2010), so the Eoembryophytic diversity changes recover the initial trends of an incipient bryophyte-like flora. From this, we see (for example) that the spore diversity curve during the Eoembryophytic phase does not show any depletion at the Hirnantian (Late Ordovician). This fact is of special relevance because it suggests that the so-called Hirnantian glaciation, responsible for the diversity depletion of many

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Fig. 3. Silurian–Mississippian genus-level megafossil-based diversity curves of lycophytes (coloured navy blue), lycopsids (sky blue), euhyllophytes (red), and ligniophytes (orange) generated from the data presented in Data S1. (A) Total observed diversity. (B) Mean standing diversity. (C) Boundary-crossing standing diversity. The diversity trajectories are scaled according to interval lengths at stage-level. White-gray boxes indicate major time intervals at epoch-level. Figure shows the apparent pattern of registered morphological diversity taken as proxy of the early plant diversity dynamics.

groups at the end of the Ordovician Period (Delabroye and Vecoli, 2010, and references therein) had little or no effect on the cryptospore-producing land plants. Notwithstanding, some authors have emphasised the great ability of the earliest land plants to grow and to reproduce under non-stable climatic conditions (e.g., Wellman and Gray, 2000). This scenario rejects any biotic crisis at the Ordovician–Silurian boundary on land ecosystems and calls into question any potential global effect of the first of the “Big Five” mass extinctions. The Eotracheophytic phase (Mid-Silurian to Early Devonian) is reflected in the dispersed spore fossil record as a continuous increase

of the genus-level standing diversity from the Sheinwoodian until the Ludfordian (Fig. 2B and C). A small reduction of the standing diversity is also detected during the Early Devonian. This dynamic embraces a key episode in vegetation history. After the Telychian, it produced the change from cryptospore to hilate/trilete spore dominance (see, e.g., Wellman et al., 2013). The trilete spore fossil record diversifies intensely during the Wenlock and continues this trend towards the Devonian (Steemans, 1999). In parallel, the cryptospore diversity declines from the Wenlock-Ludlow to the Lochkovian (Steemans, 1999). Trilete spores are produced by tracheophytes (e.g., Gray, 1985). Indeed,

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the observed pulse in spore diversity (Fig. 2) is concordant with the Rhyniophytic plant diversity pattern (Cleal and Cascales-Miñana, 2014, Fig. 5). This fact (1) suggests that the post-Telychian dispersed spore diversity was triggered by the earliest diversification of vascular plants and (2), as hypothesized by Gray (1985), supports the idea of an ecological re-emplacement of a bryophyte-dominated flora by a rhyniophytoid-dominated flora in terrestrial biota during the Mid-Late Silurian time interval. Previous works conducted at a worldwide scale have suggested a sustained increase of spore diversity during the Devonian, with a significant pulse of diversity in the Emsian and the highest value registered in the Frasnian (Chaloner, 1967, Fig. 2; Knoll et al., 1984, Fig. 1). Recent studies conducted using the South China fossil record have, in contrast, suggested three different peaks of spore diversity in the Emsian, Givetian and Famennian (Xiong et al., 2013, Fig. 1). Reported results are more in agreement with previous global patterns than the observed patterns from the South China plant fossil record. Fig. 2A shows an apparent sustained increase in spore diversity during the Devonian (Fig. 2A). Fig. 1A additionally shows a comparable pattern in the apparent standing diversity of megafossils during the Devonian. This scenario suggests a particular pattern of both microfossils and megafossils in northeastern Gondwana, where a set of sequential diversity peaks, rather a sustained increase of diversity, is observed (Wang et al., 2010; Xiong et al., 2013). This study integrates both spore and megafossil data to study the apparent early diversity trends of land plants. This strategy, although optimal in terms of involving the key diversification phases of terrestrialization process, implies the acceptance of a set of assumptions, especially in relation to the interpretation of megafossil diversity changes over time. The main problem here is that the plant fossil record rarely includes finds of complete preserved organisms. Consequently, different fossil-genera may have been generated from the same paleobiological entity. A clear example of this is the case of Wattieza givetiana, a Mid-Devonian plant from Belgium originally described by Stockmans, which belongs to cladoxylopsids (Pseudosporochnales, Meyer-Berthaud et al., 2010). Wattieza and Eospermatopteris were considered two independent plant genera until Stein et al. (2007) discovered an intact crown belonging to Wattieza and its attachment to Eospermatopteris trunk and base. This situation is especially sensitive to the calculation of post-Givetian plant diversity curves due to the expansion of the euphyllophyte clade and lycopsid diversity. In order to avoid artificially inflating diversity counts due to taxonomy, this study has tried to avoid the inclusion of genera in similar situations to Eospermatopteris by adding their temporal distribution in a single genus and removing synonymies (e.g., Rebuchia/Distichophytum or Rellimia/Protopteridium). However, in many cases these kinds of relationships are either unknown or disputed (e.g., the wood genera diversity). For this reason, the apparent megafossil-based plant diversity curves primarily represent the morphological diversity dynamics contained in the known plant fossil record. However, and interestingly, the general trend of the genus-level plant megafossil diversity pattern (especially the standing diversity, Fig. 1B) does not differ greatly from previous family-level diversity curves for the same time interval (Cleal and Cascales-Miñana, 2014), which suggests that the use of such curves as a proxy of plant diversity is not illogical. In addition, this type of approach remains useful in detecting the changes in fossil-based richness of different lineages (Fig. 3), representative of major diversity changes in past vegetation. Three important points can be derived from the comparative analysis of the apparent diversity changes of major plant lineages (Fig. 3). First, the apparently large embryophytic diversity changes (Fig. 1A) are driven by diversification within lineages (Fig. 3A) rather than by the timing of the appearance of key morphological traits. Second, all major lineages experienced a great diversification after the Mid-Late Devonian boundary (i.e., Eophytic-Palaeophytic turnover, Cleal and Cascales-Miñana, 2014, Fig. 5) (Fig. 3B and C). Third, while the standing

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Late Devonian–Mississippian lycopsid diversity curves suggest an equilibrium phase, the standing euphyllophyte diversity continued to increase during the Mississippian, driven by the expansion of lignophytes (i.e., diversification of Palaeophytic flora, Cleal and Cascales-Miñana, 2014, fig. 5; see also Decombeix et al., 2011 for further discussion) (Fig. 3B and C). Thus, this collective evidence seems to indicate that the observed plant diversity dynamics respond to the overlapping of different expansion phases of the lineages involved, in turn suggesting an intrinsic ecological control of the apparent changes in taxic richness. Fig. 3 shows, in addition, that similarly to the Ordovician–Silurian boundary, there is no evidence to support any biotic crisis at the End-Devonian in land ecosystems. If accepted, this fact suggests that the effects of the End-Devonian mass extinction would be restricted to the marine realms only. The most recent cladistic treatment resolves the vascular plant group Zosterophyllopsida as a clade unrelated to the lycophytes (Hao and Xue, 2013). Other analyses, more commonly accepted, instead consider Zosterophyllopsida to be a sister group of the lycopsids within the lycophyte clade (Kenrick and Crane, 1997a). In a recent paper, CascalesMiñana and Meyer-Berthaud (2014) traced the diversity dynamics of the Zosterophyllopsida, sensu Hao and Xue (2013). Zosterophylls were prominent components of the Early Devonian Eophytic flora (Cleal and Cascales-Miñana, 2014). This plant group experienced a great radiation during the Lochkovian, registered its heyday in the Pragian and underwent a progressive decline of diversity starting in the Emsian (Cascales-Miñana and Meyer-Berthaud, 2014). To explain this explosive diversification and the rapid decline of the group, it was hypothesized that this dynamic was the result of the competitive replacement of the zosterophyllopsids by lycopsids and basal euphyllophytes whose evolution could have been favoured by external factors (Cascales-Miñana and Meyer-Berthaud, 2015). Results presented in Fig. 3 indeed suggest that the apparent diversity pattern of lycophytes involves two different dynamics. First, we can observe a dynamic characterized by a diversity peak in the Pragian followed by a fall of the same until the Givetian (Fig. 3A). This diversity trajectory corresponds to the diversity changes of zosterophyllopsids. Conversely, we see that the lycopsid and euphyllophyte diversity patterns follow an ascending trajectory coincident with the drop of diversity in the lycophyte clade during the Emsian–Eifelian time interval (Fig. 3A). This observation (1) confirms, as expected, the change of dominance from zosterophylls to lycopsids in the post-Early Devonian fossil record and (2) suggests that the observed plant diversity depletion in the Eifelian (Fig. 1C) could be result of the overlapping of three different dynamics of diversification (i.e., zosterophyllopsids, lycopsids, and euphyllophytes) rather than only a simple sampling bias. Consequently, if we accept this view, the observed diversity patterns mirror coherent dynamics according to Sepkoski's (1978, 1979, 1984) models. This scenario seems to be advocating in favour of a conception of Zosterophyllopsida as an independent clade. On the other hand, Niklas and Tiffney commented more than 20 years ago that the quantitative studies of plant biodiversity through time were in their infancy (Niklas and Tiffney, 1994), and it is true that to some extent they continue to be in their initial phase even now. Determining the diversity of plant life is essential to our understanding of early terrestrial ecosystems. However, it is well known that the fossil-based plant diversity patterns often reflect the consequence of taphonomic process, rather than the history of past ecosystems. To address this situation, inherent in the fossil record, current tendencies in diversity studies advocate for the use of occurrencebased data counts (i.e., sampled-in-bin diversity, Alroy, 2010) rather than the standard range-based counts based on FADs-LADs. It is important to note that this study has represented only the apparent changes in the fossil diversity of land plants as part of work in progress. This allows comparison with previous works and scrutinises the reflected diversity of the fossil record. Recovered data are, in addition, useful for the reconstruction of past plant biodiversity and illustrate current

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knowledge about the temporal distribution of early floras. However, a successful interpretation of this fossil record also involves understanding its incompleteness and associated biases. For the moment, the unique available sampling-corrected diversity curves of early floras correspond to Zosterophyllopsida (Cascales-Miñana and Meyer-Berthaud, 2014, 2015). From this, it has been concluded that the great diversity fluctuations operate out of sampling bias. The work performed by Xiong et al. (2013) based on the fossil flora of South China also evaluated the sampling bias by discarding an immense effect of such bias on the interpretation of diversity dynamics. Beyond Silurian–Devonian plant diversity, a similar scenario is also described by the non-flowering seed plant diversity pattern (Cascales-Miñana et al., 2013). Thus, although we cannot dispute that the variation in the sampling intensity among the different stages can be seen as one of the weaknesses of this study, there is no current evidence to discard a priori the contention that the major apparent diversity variations, supported by both spore and plant megafossils, reflect the great turnover events of vegetation. 6. Conclusions This study has documented the apparent changes (i.e., as reflected by the known fossil record) in the diversity of plant fossils during the Ordovician–Mississippian time interval by using both spore data and plant megafossil evidence. Overall, both types of records have shown a positive trend of diversity towards the end-Devonian. Some interesting particularities have been also detected. The spore diversity pattern can be accommodated into a three-phase diversification, which responds to the earliest radiations of embryophytes (End-Ordovician to MidSilurian), tracheophytes (Late Silurian), and euphyllophytes (Mid-Late Devonian), respectively. In contrast, the megafossil-based plant diversity pattern is characterized by a set of diversity pulses in ascending order in the Pragian, Givetian, and Visean. This pattern results from the overlapping of initial expansion phases of lycophytes, early euphyllophytes, and lignophytes, respectively. Results imply that diversity patterns extracted recently from the South China plant fossil record respond to a particular dynamic of this region. Finally, evidence suggests that the plant fossil record does not support any biotic crisis in land environments neither at the Ordovician–Silurian boundary nor at the EndDevonian. The effect of the two first “Big Five” mass extinctions would therefore have been restricted to the marine realms. Acknowledgments I would like to thank Brigitte Meyer-Berthaud (AMAP, Montpellier) and Philippe Gerrienne (Dept. of Geology, University of Liege) for their helpful discussion and comments on the early diversity patterns of land plants. Thanks also to Yannick Brohard (AMAP, Montpellier) and Philippe Steemans (Dept. of Geology, University of Liege) for their technical assistance in the documentation process. Dieter Uhl (Senckenberg Research Institute, Frankfurt am Main) and Claude Monnet (CNRS, University of Lille) provided useful reviews which helped to improve an early version of this paper. This research was funded by project ANR2010-BLAN-607-02 “TERRES.” The support provided by a Marie Curie COFUND Postdoctoral Fellowship (University of Liege, grant number: 600405) is also gratefully acknowledged. Appendix A. Supplementary data Supplementary data to this article can be found online at http://dx. doi.org/10.1016/j.revpalbo.2015.10.005. References Alroy, J., 2008. Dynamics of origination and extinction in the marine fossil record. Proc. Natl. Acad. Sci. U. S. A. 105, 11536–11542.

Alroy, J., 2010. Fair sampling of taxonomic richness and unbiased estimation of origination and extinction rates. In: Alroy, J., Hunt, G. (Eds.), Quantitative methods in Paleobiology. The Paleontological Society, pp. 55–80. Anderson, J.M., Anderson, H.M., Cleal, C.J., 2007. Brief history of the gymnosperms: classification, biodiversity, phytogeography and ecology. Strelitzia 20, South African National Biodiversity Institute, Pretoria (279 pp.). Bambach, R.K., Knoll, A.H., Wang, S.C., 2004. Origination, extinction, and mass depletions of marine diversity. Paleobiology 30 (4), 522–542. Berry, C.M., Fairon-Demaret, M., 2002. The architecture of Pseudosporochnus nodosus Leclerq et Banks: a Middle Devonian cladoxilopsid from Belgium. Int. J. Plant Sci. 163 (5), 699–713. Berry, C.M., Wang, Y., Cai, C.Y., 2003. A lycopsid with novel reproductive structures from the Upper Devonian of Jiangsu, China. Int. J. Plant Sci. 164 (2), 263–273. Boltovskoy, D., 1988. The range-through method and first-last appearance data in paleontological surveys. J. Paleontol. 62 (1), 157–159. Cascales-Miñana, B., Meyer-Berthaud, B., 2014. Diversity dynamics of Zosterophyllopsida. Lethaia 47 (2), 205–215. Cascales-Miñana, B., Meyer-Berthaud, B., 2015. Diversity patterns of the vascular plant group Zosterophyllopsida in relation to Devonian palaeogeography. Palaeogeogr. Palaeoclimatol. Palaeoecol. 423, 53–61. Cascales-Miñana, B., Cleal, C.J., Diez, J.B., 2013. What is the best way to measure extinction? A reflection from the palaeobotanical record. Earth Sci. Rev. 124, 126–147. Chaloner, W.G., 1967. Spores and land-plant evolution. Rev. Palaeobot. Palynol. 1, 83–93. Chaloner, W.G., Sheerin, A., 1979. Devonian macroflora. Spec. Pap. Palaeontol. 23, 145–161. Cleal, C.J., 1993a. Plants. 43. Pteridophyta. In: Benton, M.J. (Ed.), The Fossil Record 2. Chapman and Hall, London, pp. 779–794. Cleal, C.J., 1993b. Plants. 44. Gymnospermophyta. In: Benton, M.J. (Ed.), The Fossil Record 2. Chapman and Hall, London, pp. 795–808. Cleal, C.J., Cascales-Miñana, B., 2014. Composition and dynamics of the great Phanerozoic evolutionary floras. Lethaia 47, 469–484. Crane, P.R., Herendeen, P., Friis, E.M., 2004. Fossils and plant phylogeny. Am. J. Bot. 91 (10), 1683–1699. Cressler III, W.L., Daeschler, E.B., Slingerland, R., Peterson, D.A., 2010. Terrestrialization in the Late Devonian: a palaeoecological overview of the Red Hill site, Pennsylvania, USA. In: Vecoli, M., Clément, M., Meyer-Berthaud, B. (Eds.), The Terrestrialization Process: Modelling Complex Interactions at the Biosphere–Geosphere Interface. Geological Society, Special Publications, London, pp. 111–128. Decombeix, A.-L., Meyer-Berthaud, B., Galtier, J., 2011. Transitional changes in arborescent ligniophytes at the Devonian–Carboniferous boundary. J. Geol. Soc. Lond. 168, 547–557. Delabroye, A., Vecoli, M., 2010. The end-Ordovician glaciation and the Hirnantian stage: a global review and questions about Late Ordovician event stratigraphy. Earth Sci. Rev. 98 (3-4), 269–282. Edwards, D., 1990. Constraints on Silurian and Early Devonian phytogeographic analysis based on megafossils. In: McKerrow, W.S., Scotese, C.R. (Eds.), Palaeozoic Palaeogeography and Biogeography. Geological Society Memoirs No. 12, London, pp. 233–242. Edwards, D., Wellman, C.H., 2001. Embryophytes on land: the Ordovician to Lochkovian (Lower Devonian) record. In: Gensel, P., Edwards, D. (Eds.), Plants invade the land. Evolutionary and environmental perspectives. Columbia University Press, New York, pp. 3–28. Edwards, D., Feehan, J., Smith, D.G., 1983. A Late Wenlock flora from Co. Tipperary, Ireland. Bot. J. Linn. Soc. 86, 19–36. Edwards, D., Morris, J.L., Richardson, J.B., Kenrick, P., 2014. Cryptospores and cryptophytes reveal hidden diversity in early land floras. New Phytol. 202, 50–78. Fitzgerald, P.C., Carlson, S.J., 2006. Examining the latitudinal diversity gradient in Paleozoic terebratulide brachiopods: should singleton data be removed? Paleobiology 32 (3), 367–386. Foote, M., 2000. Origination and extinction components of taxonomic diversity: general problems. Paleobiology 26 (4), 74–102. Foote, M., 2001. Inferring temporal patterns of preservation, origination, and extinction from taxonomic survivorship analysis. Paleobiology 27 (4), 602–630. Gerrienne, P., 1993. Inventaire des vegetaux eodevoniens de Belgique. Ann. Soc. Geol. Belg. 116 (1), 105–117. Gerrienne, P., Meyer-Berthaud, B., Lardeux, H., Régnault, S., 2010. First record of Rellimia Leclercq & Bonamo (Aneurophytales) from Gondwana, with comments on the earliest ligniophytes. In: Vecoli, M., Clément, M., Meyer-Berthaud, B. (Eds.), The Terrestrialization Process: Modelling Complex Interactions at the Biosphere– Geosphere Interface. Geological Society, Special Publications, London, pp. 81–92. Graham, L.E., Gray, J., 2001. The origin, morphology, and ecophysiology of early embryophytes: neontological and paleontological perspectives. In: Gensel, P., Edwards, D. (Eds.), Plants invade the land. Evolutionary and environmental perspectives. Columbia University Press, New York, pp. 140–157. Graham, L.E., Wilcox, L.W., Cook, M.E., Gensel, P., 2004. Resistant tissues of modern marchantioid liverworts resemble enigmatic Early Paleozoic microfossils. Proc. Natl. Acad. Sci. U. S. A. 101, 11025–11029. Gray, J., 1984. Ordovician–Silurian land plants: the interdependence of ecology and evolution. Spec. Pap. Palaeontol. 32, 281–295. Gray, J., 1985. The microfossil record of early land plants; advances in understanding of early terrestrialization. Philos. Trans. R. Soc. Lond. B 309, 167–195. Gray, J., 1993. Major paleozoic land plant evolutionary bio-events. Palaeogeogr. Palaeoclimatol. Palaeoecol. 104 (1-4), 153–169. Gutak, J.M., Antonova, V.A., Ruban, D.A., 2011. Diversity and richness of the Devonian terrestrial plants in the Southeastern Mountainous Altay (Southern Siberia): regional versus global patterns. Palaeogeogr. Palaeoclimatol. Palaeoecol. 299 (1-2), 240–249. Hao, S.G., Xue, J.Z., 2013. The Early Devonian Posongchong Flora of Yunnan. Science Press, Beijing (366 pp.).

B. Cascales-Miñana / Review of Palaeobotany and Palynology 227 (2016) 19–27 Hueber, F.M., Banks, H.P., 1979. Serrulacaulis furcatus gen. et sp. nov., a new zosterophyll from the lower Upper Devonian of New York State. Rev. Palaeobot. Palynol. 28, 169–189. Kennedy, K.L., Gensel, P., Gibling, M.R., 2012. Paleoenvironmental inference from the classic Lower Devonian plant-bearing locality of the Campbellton Formation, New Brunswick, Canada. Palaios 27, 424–438. Kenrick, P., Crane, P.R., 1997a. The origin and early diversification of land plants: a cladistic study. Smithsonian Institution Press, Washington (441 pp.). Kenrick, P., Crane, P.R., 1997b. The origin and early evolution of plants on land. Nature 389, 33–39. Kenrick, P., Wellman, C.H., Schneider, H., Edgecombe, D., 2012. A timeline for terrestrialization: consequence for the carbon cycle in the Palaeozoic. Philos. Trans. R. Soc. Lond. 367, 519–536. Knoll, A.H., Niklas, K.J., Gensel, P.G., Tiffney, B.H., 1984. Character diversification and patterns of evolution in early vascular plants. Paleobiology 10 (1), 34–47. Le Hir, G., Donnadieu, Y., Godderis, Y., Meyer-Berthaud, B., Ramstein, G., Blakey, R.C., 2011. The climate change caused by the land plant invasion in the Devonian. Earth Planet. Sci. Lett. 310 (3-4), 203–212. Lessuise, A., Fairon-Demaret, M., 1980. Le gisement a plantes de Niaster (Aywaille, Belgique): repere biostratigraphique nouveau aux abords de la limite CouvinienGivetien. Ann. Soc. Geol. Belg. 103, 157–181. Meyer-Berthaud, B., Soria, A., Decombeix, A.-L., 2010. The land plant cover in the Devonian: a reassessment of the evolution of the tree habit. In: Vecoli, M., Clément, M., Meyer-Berthaud, B. (Eds.), The Terrestrialization Process: Modelling Complex Interactions at the Biosphere–Geosphere Interface. Geological Society, Special Publications, London, pp. 59–70. Morris, J.L., Edwards, D., 2014. An analysis of vegetational change in the Lower Devonian: new data from the Lochkovian of the Welsh Borderland, U.K. Rev. Palaeobot. Palynol. 211, 28–54. Niklas, K.J., 1988. Patterns of vascular plant diversification in the fossil record—proof and conjecture. Ann. Mo. Bot. Gard. 75 (1), 35–54. Niklas, K.J., Tiffney, B.H., 1994. The quantification of plant biodiversity through time. Philos. Trans. R. Soc. Lond. B 345 (1311), 35–44. Niklas, K.J., Tiffney, B.H., Knoll, A.H., 1980. Apparent changes in the diversity of fossil plants. Evol. Biol. 12, 1–89. Niklas, K.J., Tiffney, B.H., Knoll, A.H., 1983. Patterns in vascular land plant diversification. Nature 303 (5918), 614–616. Niklas, K.J., Tiffney, B.H., Knoll, A.H., 1985. Patterns in vascular land plant diversification: an analysis at the species level. In: Valentine, J.W. (Ed.), Phanerozoic diversity patterns: profiles in macroevolution. Princeton University Press, New Jersey, pp. 97–128. Raymond, A., Gensel, P., Stein, W.E., 2006. Phytogeography of Late Silurian macrofloras. Rev. Palaeobot. Palynol. 142 (3-4), 165–192. Retallack, G., Landing, E., 2014. Affinities and architecture of Devonian trunks of Prototaxites loganii. Mycologia 106 (6), 1143–1158. Richardson, J.B., Edwards, D., 1989. Sporomorphs and plant megafossils. In: Holland, C.H., Bassett, M.G. (Eds.), A Global Standard for The Silurian System. National Museum of Wales, Cardiff, pp. 216–226. Rubinstein, C.V., Gerrienne, P., de la Punete, G.S., Astini, R.A., Steemans, P., 2010. Early Middle Ordovician evidence for land plants in Argentina (eastern Gondwana). New Phytol. 188, 365–369. Sepkoski Jr., J.J., 1978. A kinetic model of Phanerozoic taxonomic diversity I. Analysis of marine orders. Paleobiology 4, 223–251.

27

Sepkoski Jr., J.J., 1979. A kinetic model of Phanerozoic taxonomic diversity II. Early Phanerozoic families and multiple equilibria. Paleobiology 5, 222–251. Sepkoski Jr., J.J., 1984. A kinetic model of Phanerozoic taxonomic diversity III. PostPaleozoic families and mass extinctions. Paleobiology 10, 246–267. Steemans, P., 1999. Paléodiversification des spores et des cryptospores del'Ordovician au Dévonien Inférieur. Geobios 32, 341–352. Steemans, P., 2000. Miospore evolution from the Ordovician to the Silurian. Rev. Palaeobot. Palynol. 113, 341–352. Steemans, P., Wellman, C.H., 2004. Miospores and the emergence of land plants. In: Webby, B.D., Paris, F., Droser, M.L., Percival, I.G. (Eds.), The Great Ordovician Biodiversifi cation Event. Columbia University Press, New York, pp. 361–366. Steemans, P., Wellman, C.H., Gerrienne, P., 2010. Palaeogeographic and palaeoclimatic considerations based on Ordovician to Lochkovian vegetation. In: Vecoli, M., Clément, M., Meyer-Berthaud, B. (Eds.), The Terrestrialization Process: Modelling Complex Interactions at the Biosphere–Geosphere Interface. Geological Society, Special Publications, London, pp. 49–58. Steemans, P., Petus, E., Breuer, P., Mauller-Mendlowicz, P., Gerrienne, P., 2012. Palaeozoic Innovations in the Micro- and Megafossil Plant Record: From the Earliest Plant Spores to the Earliest Seeds. In: Talent, J.A. (Ed.), Earth and Life, International Year of Planet Earth. Springer-Science and Business Medisa B.V, pp. 437–477. Stein, W.E., Mannolini, F., Hernick, L.V., Landing, E., Berry, C.M., 2007. Giant cladoxylopsid trees resolve the enigma of the Earth's earliest forest stumps at Gilboa. Nature 446 (7138), 904–907. Strother, P., Lenk, C., 1983. Eohostimella is not a plant. Am. J. Bot. 70, 80. Tomescu, A.M.F., 2009. Megaphylls, microphylls and the evolution of leaf development. Trends Plant Sci. 14, 5–12. Vecoli, M., Meyer-Berthaud, B., Clément, G., 2010. The terrestrialization process: modelling complex interactions at the biosphre-geosphere interface-Introduction. In: Vecoli, M., Clément, M., Meyer-Berthaud, B. (Eds.), The Terrestrialization Process: Modelling Complex Interactions at the Biosphere–Geosphere Interface. Geological Society, Special Publications, London, pp. 1–3. Wang, D.M., Hao, S.G., Wang, Q., 2005. Rotafolia songziensis gen. et comb. nov., a sphenopsid from the Late Devonian of Hubei, China. Bot. J. Linn. Soc. 148 (1), 21–37. Wang, Y., Wang, J., Xu, H., He, X., 2010. The evolution of Paleozoic vascular land plant diversity of South China. Sci. China Earth Sci. 53 (12), 1828–1835. Wellman, C.H., 2010. The invasion of the land by plants: when and where? New Phytol. 188, 306–309. Wellman, C.H., Gray, J., 2000. The microfossil record of early land plants. Philos. Trans. R. Soc. Lond. B 355, 717–732. Wellman, C.H., Osterloff, P.L., Mohiuddin, U., 2003. Fragments of the earliest land plants. Nature 425, 282–285. Wellman, C.H., Steemans, P., Vecoli, M., 2013. Palaeophytogeography of Ordovician– Silurian land plants. In: Harper, D.A.T., Servais, T. (Eds.), Early Palaeozoic Biogeography and Palaeogeography. Geological Society, London, pp. 461–476. Xiong, C., Wang, D.M., Wang, Q., Benton, M.J., Xue, J.Z., Meng, M., Zhao, Q., Zhang, J., 2013. Diversity dynamics of Silurian–early carboniferous land plants in South China. PLoS ONE 8 (9), e75706. Xue, J., Huang, P., Ruta, M., Benton, M.J., Hao, S., Xiong, C., Wang, D., Cascales-Miñana, B., Wang, Q., Liu, L., 2015. Stepwise evolution of Paleozoic tracheophytes from South China: contrasting leaf disparity and taxic diversity. Earth Sci. Rev. 148, 7–93.