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How Green Was Cooksonia? the Importance of Size in Understanding the Early Evolution of Physiology in the Vascular Plant Lineage

How Green Was Cooksonia? the Importance of Size in Understanding the Early Evolution of Physiology in the Vascular Plant Lineage

Paleobiology, 34(2), 2008, pp. 179–194

How green was ? The importance of size in understanding the early evolution of physiology in the vascular lineage

C. Kevin Boyce

Abstract.—Because of the fragmentary preservation of the earliest Cooksonia-like terrestrial plant macrofossils, younger with complete anatomical preservation and documented often have received greater attention concerning the early evolution of vascular and the alternation of generations. Despite preservational deficits, however, possible phys- iologies of Cooksonia-like fossils can be constrained by considering the overall axis size in con- junction with the potential range of cell types and sizes, because their lack of organ differentiation requires that all plant functions be performed by the same axis. Once desiccation resistance, sup- port, and transport functions are taken into account, smaller fossils do not have volume enough left over for an extensive aerated photosynthetic tissue, thus arguing for physiological dependence on an unpreserved . As in many , axial anatomy is more likely to have ensured continued dispersal despite desiccation of the than to have provided photosyn- thetic independence. Suppositions concerning size constraints on physiology are supported by size comparisons with fossils of demonstrable physiological independence, by preserved anatomical detail, and by size correlations between axis, sporangia, and sporangial stalk in and Early Devonian taxa. Several Cooksonia-like taxa lump fossils with axial widths spanning over an of magnitude—from necessary physiological dependence to potential photosynthetic compe- tence—informing understanding of the evolution of an independent sporophyte and the phylo- genetic relationships of early vascular plants.

C. Kevin Boyce. Department of the Geophysical Sciences, University of Chicago, 5734 South Ellis Avenue, Chicago, Illinois 60637. E-mail: [email protected]

Accepted: 22 January 2008

Introduction ler and Churchill 1985; Rothwell 1995). That Much is unknown about the ecology and cooksonioid fossils are small but relatively in- physiology of the oldest preserved macrofos- tact is supported by their uni- sil land plants. These cooksonioid fossils first form size in beds containing many fossils and appear in the Wenlockian (Edwards and Fee- by spore morphologies distinct from the larg- han 1980; Edwards et al. 1983) and remain a er taxa of which they could conceivably be dis- common component of the paleoflora through tal fragments (Edwards 1996). Their most the rest of the Silurian and the Early Devonian common treatment is an intermediate one in (Edwards 1973, 1979a). These fossils consist of which the plants are considered small and de- unadorned axes that can branch isotomously, terminate but without implication of gameto- are terminated by sporangia, and are quite phyte dependence for rooting and substrate small—often of mesofossil proportions. The interaction (Edwards and Fanning 1985; Ed- small size of the axes and their limited num- wards 1996). (Originally reflecting equivocal ber of dichotomies has led to distinct inter- evidence for vasculature [Taylor 1988] and pretations of plant habit, ranging from the fos- similar to the more common ‘‘rhyniophytoid’’ sils representing determinate, aerial axes bro- [Edwards 1996], ‘‘cooksonioid’’ here denotes ken from indeterminately growing only simple, smaller taxa usually less than 1 not preserved (Niklas 1997; Kenrick and Davis mm in width and lacking signs of indepen- 2004) to complete, determinate sporophytes dent growth described below, thereby includ- rooted in a gametophyte, although without ing Cooksonia, Salopella, Tarrantia, Tortilicaulis, discussion of whether sporophyte physiolog- but excluding larger fossils such as Aglaophy- ical dependence extended beyond water and ton.) nutrient acquisition from the substrate (Mish- Despite their obvious centrality for under-

᭧ 2008 The Paleontological Society. All rights reserved. 0094-8373/08/3402-0002/$1.00 180 C. KEVIN BOYCE standing the early evolution of the vascular was based upon axes of 1 mm diameter and plant lineage, the importance of these cook- then generalized to other taxa. Furthermore, sonioid fossils has in many ways been over- these calculations were ultimately limited by whelmed by the abundance of information a lack of anatomical detail: in modeling pho- from the Lower Devonian of tosynthetic assimilation, only the endpoints of

Scotland, almost 50 Myr younger than the old- the CO2 diffusion pathway were considered, est cooksonioids. The Rhynie Chert provides whereas inclusion of progressive CO2 deple- the earliest detailed anatomy (Edwards 1993) tion with loss to cells intermediate between for a diverse flora (Kidston and Lang 1917, the stomata and the innermost chlorenchyma 1920a,b; Lyon and Edwards 1991; Powell et al. is crucial (Konrad et al. 2000; Roth-Nebelsick 2000; Kerp et al. 2001), which has in turn in- and Konrad 2003). Similar problems can be ex- formed phylogenetic understanding (Gensel pected with hydraulic calculations for which 1992; Kenrick and Crane 1997) and allowed proximal water loss can be a far greater con- well-constrained modeling of physiological cern (Zwieniecki et al. 2004, 2006) than pro- function (Konrad et al. 2000; Roth-Nebelsick vided for by the assumption in early studies 2001; Roth-Nebelsick and Konrad 2003), to- of linear water loss along the axis. gether indicating an ancestral condition with Because anatomical context has proven es- little tissue diversity or organ differentiation sential, recent modeling necessarily has been but general photosynthetic and physiological limited to permineralized fossils. In the fu- continuity with later vascular plants. The Rhy- ture, techniques such as X-ray computed to- nie Chert also has yielded axial gametophyte mography (Tafforeau et al. 2006) might pro- fossils that are predominantly of equivalent vide greater anatomical information from tissue complexity and size to the correspond- cooksonioid mesofossils than is provided by ing sporophyte (Remy 1982; Remy et al. 1993; the current reliance on surficial exposure and Kerp et al. 2004; Taylor et al. 2005), thereby im- intentional breakages (Edwards and Axe plying that all land plants (Remy 1982) or at 2000). However, even if the detailed physio- least vascular plants (Kenrick 2000) diverged logical consideration received by Rhynie fos- from a common ancestor with equal genera- sils and other early permineralized plants tions, as opposed to following the trend from (Edwards et al. 2006) currently cannot be rep- gametophyte to sporophyte dominance ex- licated for the anatomically incomplete cook- pected from the characteristics and relation- sonioid compressions and mesofossils, their ships of living land plants. preservation may yet be sufficient to constrain Although available anatomy has been de- what physiologies would not have been pos- scribed for individual cooksonioid specimens, sible. the preservation of that anatomy is partial and gametophyte fossils are unknown. As a result, Size Constraints on Tracheophyte in syntheses of early evolutionary patterns, Physiological Independence cooksonioids are often atomized and serve as Plant Function and Division of Labor. The mileposts for the accumulation of individual functions essential for nearly all independent- characteristics (e.g., Banks ly growing terrestrial plants—desiccation re- 1981; Knoll et al. 1984; Niklas 1997; Edwards sistance, structural support, hydraulic and 2003), leaving unresolved the implication that solute transport, and —can the general continuity with modern sporo- have contradictory requirements and necessi- phyte photosynthetic function demonstrable tate segregation into distinct tissues. For ex- in the Rhynie Chert persists in the still deeper ample, photosynthesis is severely limited if past despite the greater morphological sim- photosynthetic cells do not have direct access plicity of the fossils. to airspaces because CO2 diffusion is much Such continuity was supported by early more rapid through air than water (Raven modeling efforts upholding photosynthetic 1996); however, the epidermis must have con- independence of early vascular plant sporo- tiguous, cuticle covered cells if it is to act as a phytes (Raven 1984, 1993). However, that work barrier to water loss. Mechanical and hydrau- HOW GREEN WAS COOKSONIA? 181 lic functions can be similarly compromised by intercellular airspaces. In all Silurian and Early Devonian plants except , these mutually ex- clusive functions must be performed by (and all discrete tissues contained within) the axis as the only vegetative organ (Edwards 1993), placing geometric constraints and potentially a minimum viable size upon that axis. Mini- mum size constraints are easy to overlook be- cause diverse, small structures are abundant in more complex vascular plants, but they rep- resent specializations for limited functions. For example, the rachis of a maidenhair frond can be less than 500 ␮ thick, but is not photosynthetic and does not require airspac- es. The axes of early fossil plants could not eas- ily circumvent these functions and resulting tissue requirements. For example, the mycor- rhizal fungi seen in the Rhynie Chert (Taylor et al. 1995, 2004) would simplify the addition- al requirement of nutrient acquisition from the substrate, but would not affect any of the aboveground functions discussed here. Also, if a transpiring axis simply did not have vas- culature, then it would lose too much water proximally and have inadequate transport rates along the axis to support distal tissues because of the high hydraulic resistance of symplastic and apoplastic transport through parenchyma (Zwieniecki et al. 2004); even the small sporophyte axes of mosses typically FIGURE 1. Size constraints on axial anatomy. A, Sche- matics of tissue distribution in axial cross-sections for have dedicated conducting cells (He´bant 1977; and Devonian . B, Proportional Crum 2001). occupation of cross-sectional area calculated in cylin- drical axes of different thicknesses for concentric tis- Psilotum sporophytes, in which a leafless sues. For calculations, the arrangement was axis is the solitary vegetative organ , pro- used, with stereome immediately adjacent to epidermis vides the best extant analogue of early vas- and chlorenchyma more deeply seated, rather than the Psilotum arrangement with chlorenchyma between epi- cular plants. Psilotum axes consist of a series dermis and support tissues. C, Minimum axial size in of concentric tissues fulfilling discrete func- Silurian and Early Devonian taxa demonstrating sub- tions; from periphery to center, they are epi- strate interaction through rhizoids, rhizomatous growth, or other rooting structures, and thereby dem- dermis for protection and desiccation resis- onstrating physiological independence from the game- tance, aerated chlorenchyma for photosynthe- tophyte generation. sis, sclerenchymatous stereome for - based structural support, parenchyma for mensions similar to axial plants from the Rhy- hydrostatic-based structural support, and nie Chert. central vasculature for transport (Fig. 1A). Geometric Constraints on Axial Tissues. For These tissues are housed in a cylindrical axis plants with an axial organization similar to 2 to 3 mm in diameter that can range down to Psilotum or Rhyniophytes, the minimum func- about 1 mm wide in the distal segments—di- tional size can be inferred from the minimum 182 C. KEVIN BOYCE cell sizes and volume occupation of different sents a peripheral skin that cannot be engaged tissue types. Although as large as 140 ␮ by the in photosynthesis. (Similar limitations also end of the Devonian, smaller water-conduct- apply to internal tissues lacking airspaces.) ing tracheid cells are 8–10 ␮ in diameter (Nik- Furthermore, epidermal contact with internal las 1985). However, tracheids cannot be fes- airspaces would be precluded in axes possess- tooned across airspaces; maintenance of a ing a stereome or other hypodermal tissues continuous surrounding layer of cells is need- (Fig. 1A), so that photosynthesis would not be ed for radial apoplastic transport. This sheath available in the peripheral tissues of many Si- typically occupies a much larger volume than lurian and Devonian taxa (Edwards et al. the actual conducting cells (Armacost 1944). 1996). Depth of light penetration is not a con- Phloem also requires associated nonconduct- cern in itself; however, less and less volume is ing cells for maintenance of and the loading available with greater depth within the axis— and unloading of solutes into the conducting particularly as the surface area to volume ratio cells. Therefore, a minimized stele with increases with decreasing size. Hydrostatic and phloem each represented by a single con- support represents another demand upon ax- ducting element would still likely have a 40 ␮ ial volume not accounted for in Figure 1B, al- minimum diameter once the investing layer of though the non-transporting cells on the pe- nonconducting cells is included. The epider- riphery of the vasculature may grade into a mis can be a single layer of cells that are often larger hydrostatic support tissue. As exam- as little as 10–20 ␮ thick (although cell thick- ples, volume occupation of chlorenchyma and nesses of Ͼ100 ␮ also are known among Early central hydrostatic tissues are 16% and 69%, Devonian examples [e.g., Kerp et al. 2001]). respectively, for and 20% and 59% Requirements for stereome structural support for (estimated from Edwards 1993; will depend upon the dimensions of the axis Roth-Nebelsick and Konrad 2003). (Niklas 1997). In the smaller axes for which a Other studies have tried to set theoretical stereome has been demonstrated, that tissue is minimum plant sizes on the basis of maxi- approximately three cell layers and 50 ␮ thick mally efficient packing of minimally sized including the epidermal layer (Edwards et al. cells (Raven 1999), but these were intended for 1986). rough estimations of photosynthetic output The geometric limitations on small axial rather than full consideration of all plant func- plants become clear if the cross-sectional area tions including transport and mechanical sup- occupied by the minimal thicknesses dis- port or of documented anatomical constraints cussed above for concentric vasculature, ster- such as peripheral tissues being unavailable eome, and epidermis is calculated for cylin- for photosynthesis (Edwards et al. 1996). The drical axes of different diameters (Fig. 1B). Be- calculations here (Fig. 1B) emphasize that cause the vasculature is central in the axis, it many plant functions require a trivial propor- occupies little proportional volume except in tion of axial volume in even modestly sized axes Ͻ200–300 ␮ in diameter. However, the axes, but each function represents an increas- peripheral epidermis and stereome require- ingly significant constraint with axial diame- ments rapidly begin to crowd out other tissues ters much less than 1 mm—a challenge com- as the surface area to volume ratio increases in pounded if all functions must be performed in axes narrower than approximately 800 ␮. a single axis—providing a baseline for com- Photosynthesis and hydrostatic support re- parison to axial sizes in the early fossil record. quire additional tissues. Although the epi- dermis is photosynthetic in some shade plants Methods (Esau 1953), particularly (Ogura 1972), Dimensions of Silurian and Early Devonian chloroplasts are limited to portions of the cell fossil plants were compiled from the litera- in contact with mesophyll airspaces because ture. Unless unbranched, minimum and max- aqueous diffusion of CO2 more than a couple imum axial diameter for all taxa were mea- of microns is prohibitively slow (Raven 1996). sured in between dichotomies on relatively Therefore, the bulk of the epidermis repre- straight axial portions; maximum diameters HOW GREEN WAS COOKSONIA? 183 thereby exclude the axial swelling that is com- of 0.9 mm would be used for a that mon proximal to incipient dichotomies or to bears rooting evidence on 2.0-mm-wide rhi- sporangia and minimum diameters exclude zomes if its aerial axes taper to 0.9 mm) limits sterile terminal segments that can taper sig- the taphonomic risk of size constraints being nificantly. Sporangial length and width were inflated by the preferential fragmentation of also measured (along with the third dimen- smaller aerial axes. The unlikelihood that rhi- sion, when available), as was minimum spo- zoids will be preserved without perminerali- rangial stalk width for non-terminal sporan- zation presents a second taphonomic concern; gia. Sterile form taxa (e.g., Hostinella) and frag- however, there is still ample evidence for in- ments were excluded unless they possessed determinate growth without it and few taxa characteristics such as H- or K-branching use- (e.g., ) are recognized as inde- ful for analyses described in following sec- pendent based upon rhizoids alone. Evidence tions. of physiological independence is abundant in Ranges and means tabulated in the litera- taxa with axes as small as 0.8 mm, but the ture were used when available; otherwise, smallest with such evidence is 0.7 mm (Fig. measurements were made directly from fig- 1C)—results that are consistent with esti- ured specimens. Measurements were lumped mates that the geometric constraints of tissue as size ranges for each species (Appendix 1 packing become prohibitive in axes much online at http://dx.doi.org/10.1666/07056. smaller than 1 mm (Fig. 1B). s1) except where amplified with measurement Size Range of Silurian and Early Devonian records for individual figured specimens of Plant Fossils. Most taxa conform to the size cooksonioids (Appendix 2). In comparative limits implied by both estimation of geometric analyses, midpoint values between the maxi- constraints and morphological proxies for in- mum and minimum were used when mean dependence (Fig. 1). However, cooksonioid values were not available. taxa can range down well below 100 ␮ in axial diameter, and individual genera (Fig. 2) or Size and Habit of Early Land Plant Fossils even morphospecies (Fig. 3) can span almost Minimum Sizes of Fossils with Demonstrable two orders of magnitude, straddling the in- Physiological Independence. Beyond coarse ferred physiological size threshold. This ex- geometric constraints (Fig. 1B), the distribu- treme variance reflects that size has not been tion of morphological characteristics across a direct criterion for . The likelihood the size range of fossils may provide addition- has been widely discussed that Cooksonia and al evidence concerning minimum viable axis other morphotaxa that are based only upon diameters. The presence of , rhizoids, or few and simple characteristics may artificially indeterminate rhizomatous growth (reviewed group fossils that are not closely related (Ed- in Gensel et al. 2001; Raven and Edwards wards 1979b; Taylor 1988; Fanning et al. 1992; 2001; Kenrick 2002; Boyce 2005) demonstrates Edwards et al. 2001; Habgood et al. 2002); size substrate interaction without a gametophyte may prove a valuable additional characteristic intermediary and thereby independent phys- for parsing fossils with such simple morphol- iological existence. For example, Rhynie Chert ogies. tracheophytes and protracheophytes—all of Size extremes are unlikely to reflect taphon- roughly similar axis diameter to extant Psilo- omy alone. Many cooksonioids are preserved tum (Appendix 1)—possess rhizoids (Aglao- as charcoal (Edwards 1996; Glasspool et al. phyton, Horneophyton, Rhynia), other rooting 2006), which can entail shrinkage (e.g., Glas- structures (), or rhizomatous spool et al. 2006: Plate 1.7). However, this growth (Aglaophyton, Asteroxylon, , Rhy- shrinkage is typically in the range of 14–47% nia) (Kidston and Lang 1920b, D. S. Edwards (Lupia 1995) and hence not relevant here; at 1980, 1986; Gensel et al. 2001; Kerp et al. 2001). issue are not axial widths of 100 versus 150 ␮, Minimum axis sizes for species with de- but rather 100 ␮ versus 1 mm. Instead, the siz- monstrable independence are plotted in Fig- es of cooksonioids must be interpreted as a ure 1C. Use of minimum diameter (i.e., a value genuine physiological dilemma. Regardless of 184 C. KEVIN BOYCE

FIGURE 2. Range in axial diameters for Silurian and Early Devonian genera. HOW GREEN WAS COOKSONIA? 185

do squarely occupy the smaller end of the nor- mal range. Some examples of smaller cells are known from cooksonioids–significantly all represent central, thick-walled cells for which pro- grammed cell death may have come before the vacuolate expansion that characterizes other cell types. For such anatomical curiosities as ‘‘vasculature’’ almost occluded by thickenings (Edwards 2000) or only 2 ␮ wide (Edwards et al. 1992), identifying function is difficult (Ed- wards 2003). Water-conducting cells are often spindle shaped, and some of these examples likely reflect the tapering ends of larger ele- ments (Edwards and Axe 2000). Using as a guide, limited op- FIGURE 3. Range in axial diameters for morphospecies of particularly variable cooksonioid genera. portunities do exist for the exclusion of entire tissue types. External transport through cap- illary action along enation bases obviates the how their biology is ultimately interpreted, need for internal vasculature in many continuity with later vascular plant process- gametophytes (and can actually proceed fast- es—just on a smaller scale—is problematic. er than internal transport in mosses that have both methods available [reviewed in He´bant Physiological Independence Despite 1977]). However, external transport would not Small Size be available to the unadorned axes of cook- Various mechanisms, all involving extreme sonioids, as is also the case for moss sporo- departures from known tracheophyte biology, phytes typically containing hydrome and/or can be envisioned to allow photosynthetic in- leptome analogues of tracheophyte xylem and dependence in very small plants; however, phloem. Additionally, bryophytes possess none are likely to apply to cooksonioids. If cell highly divergent modes of sporophyte size were greatly reduced, that could allow growth—the basal growth of , the rhyniophyte-like tissue complexity in a small- delayed tissue expansion of liverworts only er axis. However, those smaller cells would after differentiation is complete, the tiered dis- probably have to average 1 ␮ or less in diam- tal growth seen in bryopsid mosses in which eter in cooksonioid axes that can be much less apical tissue is set aside early for sporangial than 100 ␮ wide. The absence of vacuoles im- differentiation and seta elongation progresses plied by such small cell size would represent from more proximal tissue, and the lack of the highly unusual loss of a fundamental as- sporophyte growth beyond the sporangia it- pect of land plant biology that would be coun- self in other mosses (Crandall-Stotler 1980; terproductive as far as the cost of dry-matter Renzaglia et al. 2000; Crum 2001)—all of investment (Raven 1999). Regardless, the cells which should minimize the need for nutrient of cooksonioid plants are of normal size, typ- transport to growing sporophyte tissues. ically 10–20 ␮, when preserved (Edwards et However, the branching seen in cooksonioid al. 1986, 1992, 1994; Fanning et al. 1992; Ed- axes would not be possible without apical wards 2000; Habgood et al. 2002). Cookson- growth (Kenrick discussion in Edwards 2000), ioids obviously cannot express the larger end and so none of these growth modes of the size range, because some en- would be possible (except perhaps for un- tire cooksonioid axes are narrower than the 60 branching Tortilicaulis specimens for which a to 120 ␮ width common for individual paren- liverwort affinity has been considered [Ed- chyma and epidermis cells of Rhynie Chert wards 1979b]). Furthermore, both external fossils (e.g., Kerp et al. 2001); nonetheless, they transport and divergent growth strategies 186 C. KEVIN BOYCE would each only limit the need for vascula- the need to survive such transient threats is ture, which already takes up little volume be- not consistent with the overall cooksonioid cause of its central axial location (Fig. 1) and morphology of determinate growth in a her- which is indeed already known from many baceous plant at most a few centimeters tall mesofossils—cooksonioid (Edwards et al. with a uniquely exposed apical meristem. 1992; Edwards and Axe 2000; Edwards 2003; Such a plant might be better adapted for stress Glasspool et al. 2006) and otherwise (Edwards avoidance with life-cycle completion only dur- 2000). ing favorable conditions. UV and other envi- In the absence of a cuticle, axial surface area ronmental threats are more constant, but the could be available for photosynthesis (Raven cuticle, anthocyanins, and other aspects of 1993) and internal airspaces be avoided. How- plant biochemistry (Edwards et al. 1996; Ra- ever, the cylindrical morphology of cookson- ven 2000) are involved in UV absorption be- ioid axes minimizes external surface area and yond the presumed lignin (Niklas 1976; Ed- they are seen to have tightly packed epidermal wards et al. 1997; Boyce et al. 2003) of ster- cells when cell outlines are preserved (e.g., eome cell walls. Furthermore, protection af- Edwards and Wellman 2001), so that photo- forded by differentiated stereome would only synthesis would thereby be restricted to only be available to more proximal, mature tissues, that limited axial surface. Cooksonioid taxa whereas it is the growing apex that likely show none of the elaboration of external pho- would be the most vulnerable. Finally, mono- tosynthetic surface area common to liverwort carpic plants typically die after reproduction; and moss gametophytes (Renzaglia et al. there is no value to continued axial activity 2000) and instead resemble other members of once the terminal sporangia are mature. As a the tracheophyte lineage for which the norm result, the sterome of the small, determinate is internalization of what photosynthetic spac- cooksonioids represents such a prohibitive in- es are present. vestment of axis volume and thickened cell The one entirely expendable tissue is a hy- wall biosynthesis that it must have played a podermis or stereome; plant axes in the size role distinct from that in larger, indetermi- range of smaller cooksonioid axes can rely ex- nately growing plants. Even if the stereome is clusively on turgor from the hydrostatic core deemed homologous as an anatomical struc- (Niklas 1997). Nonetheless, a stereome is pre- ture between Cooksonia and , its served in some of the narrowest cooksonioids function was likely distinct. (Edwards et al. 1992; Fanning et al. 1992; Ed- The stereome documented in cooksonioids wards 2000). In order to account for their has been treated as a link to more complex tra- small size, the only function available to ex- cheophytes and a pteridophytic lifestyle (Ed- clude may be photosynthesis. wards et al. 1986; Kenrick and Crane 1997) (al- though other cooksonioid characteristics have An Alternative Interpretation of been treated with increasing circumspection, Cooksonioid Biology owing to their prevalence in some bryophytes Significance of Hypodermal Tissues. In ad- [Edwards 2000]); however, 60% of the volume dition to mechanical support (Niklas 1976; of the fossil in question is taken up by a ster- Edwards and Fanning 1985; Edwards 1996), eome that is not needed for structural support the stereome preserved in many cooksonioid in a hydrostatic plant with a 150 ␮ diameter axes (but not all [Edwards and Axe 2000]) has and that is of questionable alternative utility. been interpreted as an adaptation to resisting Furthermore, chlorenchyma at least has the drought (Edwards and Fanning 1985; Ed- volume advantage of being more peripheral wards et al. 1986) and potentially could have than the sclerenchyma in Psilotum, but the op- shielded the plant from ultraviolet light or posite is true in early land plants (Fig. 1A), other environmental threats (Raven 1984). Re- making a stereome in such volume-con- gardless of the potential efficacy of a stereome strained plants all the more problematic. Giv- for withstanding drought in larger plants en the vascular and peripheral anatomy pre- such as Psilophyton (e.g., Edwards et al. 1997), served, smaller cooksonioid axes likely would HOW GREEN WAS COOKSONIA? 187 not have had the capacity for an extensive, aer- ated photosynthetic tissue—suggesting in- stead photosynthetic dependence on an un- preserved gametophyte. An explanation for cooksonioid function may best be afforded by the wiry setae of mosses where stereome allows the sporophyte to remain erect after axis desiccation because spore dispersal is more efficacious in dry air (Edwards 1996; Crum 2001). For taxa in which dehiscence may have been dependent on spo- rangial drying (Edwards et al. 1996) or which show no specialized dehiscence mechanism and appear dependent on general sporangial wall disintegration (Edwards 1996; Habgood et al. 2002), maintaining axes erect postmor- tem may have been particularly important. Rather than hardy survivors pioneering both the terrestrial landscape and the overall phys- iological strategy so successfully exploited by later vascular plants, smaller cooksonioid spo- rophytes more likely represent ephemeral, ga- metophyte-dependent reproductive struc- tures with an anatomical construction allow- ing continued spore dispersal after sporo- phyte death. Size Correlations Involving Sporangia. The scaling of size of with that of spo- rangial stalk and supporting axis can provide an independent assessment of photosynthetic FIGURE 4. Correlation of sporangial volume with cross- potential. In trimerophytes and , sectional area of non-cooksonioid axes presumed to be the axes upon which sporangia are borne can photosynthetic (A), of sporangial stalks presumed to be poorly photosynthetic (B), of cooksonioid axes (C), and be expected to have fulfilled all plant func- of all subtending axes in composite (D). Calculations tions including photosynthesis, whereas the based upon mean or midpoint values for species except short stalks connecting sporangium to axis where amplified in cooksonioids with measurements of individual specimens. were much less likely to have been signifi- cantly photosynthetic and instead probably were involved only in the structural and vas- phological solutions for the diverse functions cular support of the sporangia. As such, for a of these axes (Niklas 1997). particular sporangium size, sporangial stalks Among non-cooksonioid Silurian and Early typically should be substantially thinner than Devonian taxa, the above expectations are the photosynthetic main axes because of the borne out: relative to photosynthetic axes, the fewer functions being performed (and fewer cross-sectional area of sporangial stalks is tissues types needed). Also, sporangial stalk smaller and more tightly correlated with spo- size should show close correlation with spo- rangial volume (Fig. 4). Sporangia were treat- rangium size because the limited number of ed as ellipsoids to estimate sporangial vol- straightforward functions of the stalk are all ume. Where unknown, the third sporangial directly related to the sporangia; the scaling of dimension was estimated as the lesser of the sporangial size with the main axis, on the oth- two known dimensions; i.e., depth was as- er hand, should show more variance because sumed to equal width in fusiform sporangia of the more complex array of suboptimal mor- and length in most reniform sporangia. (The 188 C. KEVIN BOYCE volume of some of the more discoidal zoster- Discussion), but axial and sporangial dimen- ophyll sporangia will be overestimated by this sions support interpretation of all smaller method.) Axis width is measured at the point cooksonioid sporophytes as organs of sporan- of sporangial attachment rather than repre- gial support rather than of photosynthesis. senting the overall range in axis size for the Significance of Stomata. Several cookson- whole plant. For estimates of cross-sectional ioid axes have preserved stomata (Edwards et area from preserved widths, axes and sporan- al. 1986, 1994; Edwards 1996; Habgood et al. gial stalks were assumed to be cylindrical. 2002), a clear indication of regulated internal Axes grossly departing from this shape (e.g., gas exchange. Although often essentially syn- Huvenia or Serrulacaulis) were excluded from onymous with photosynthesis in living vas- the analysis, as were individual measure- cular plants, the presence of stomata is not, ments involving sessile, sunken, or otherwise however, inconsistent with limited or no pho- obscured sporangial attachment or for which tosynthetic capability. Because the transport physiology is ambiguous (e.g., branching Le- of solutes through the xylem is reliant upon clerqia sporophylls). -driven flow, stomata may have If photosynthetic, then the axis/sporangi- been necessary before playing a role for pho- um size scaling of cooksonioids should be tosynthetic gas exchange, in increasing tran- similar to that of larger photosynthetic axes spiration and thereby increasing xylem nutri- although extending into a much smaller size ent flux (Edwards et al. 1996). Stomata can be range. If cooksonioid axes were not extensive- considered a clear indicator of a cuticular bar- ly photosynthetic, but instead were involved rier to evaporation, but not necessarily pho- primarily in sporangial mechanical and vas- tosynthesis. cular support, then their size scaling should When preserved in cooksonioid fossils, sto- more closely resemble that of the sporangial mata are often concentrated distally at the stalks of larger plants rather than photosyn- base of the sporangium where they are some- thetic axes. For cooksonioid specimens, spo- times associated with a swollen neck of tissue rangial volume and axis cross-sectional area (Edwards 1996; Edwards et al. 1996, 1998), a were estimated as described above with the pattern that is shared with many moss spo- exception that the axis width used was the me- rophytes (Edwards 1996, 2000). The differen- dian value between proximal and distal ex- tiation of these distal stomata may have pro- tremes (except for any swelling immediately vided an increase of transpiration-mediated proximal to a sporangium). solute delivery to the apex just when a spo- The correlation of cooksonioid axis and spo- rangium was initiated and required an in- rangium size closely resembles that of the creased nutrient flux (Edwards et al. 1996). sporangial stalks of large photosynthetic This stomatal distribution may also have been plants rather than that of the photosynthetic important for photosynthesis; when present, a axes (Fig. 4). Although they include smaller sporangial neck tends to be the widest part of cross-sectional areas, their axis/sporangial the axis and hence possesses the greatest ca- size ratios overlap with those of sporangial pacity for possible airspaces and chlorenchy- stalks—with which they also share similar ma. This is borne out in some moss sporo- slopes and variance—while being shifted sub- phytes that have highly elaborate air chambers stantially away from the range of photosyn- in the dilated tissues adjacent to and enclosing thetic axes toward smaller axial size for a par- the sporangial cavity (e.g., Splachnum or Fu- ticular sporangial volume. [The relative small- naria of the or various Polytrichidae ness of cooksonioid axes for their sporangial [Crum 2001]). In addition to any role these air- sizes may be even more pronounced than spaces may play in reproduction and spore shown here because of the overestimation of dispersal, these mosses can possess substan- sporangial volume discussed tial—but still insufficient—photosynthetic ac- above.] A few of the largest cooksonioid axes tivity (Bold 1940; Paolillo and Bazzaz 1968; do overlap with the size ratios of photosyn- Proctor 1980; Renzaglia et al. 2000). thetic axes (as commented upon below in the Although the sporangial neck may well HOW GREEN WAS COOKSONIA? 189 have been a localized site of photosynthetic indicated by the following three observations: production, all but the distalmost axial epi- (1) the lack of a multicellular sporophyte dermis in these cooksonioids has a very low among the Charales sister group to the land stomatal density. The generally low stomatal plants; (2) the extremely divergent mecha- densities of Early and Middle Devonian fos- nisms of sporophyte growth between liver- sils is attributed to high atmospheric CO2 worts, hornworts, mosses, and vascular (McElwain and Chaloner 1995; Edwards et al. plants; and (3) the paraphyletic nature of the 1998); however, cooksonioid stomatal densi- bryophytes relative to the tracheophytes ties are low even by Devonian standards: (Mishler and Churchill 1984, 1985; Hemsley when stomata are not absent, cooksonioids 1994; Kenrick 1994, 2000; Renzaglia et al. typically possess about 1 /mm2 (Ed- 2000). As essential as that work has been in es- wards 1996), whereas most other Early De- tablishing sporophyte origins, such inference vonian sporophytes range from 3 to 31.5 sto- from the phylogeny of living plants cannot in- mata/mm2 (McElwain and Chaloner 1995; form the timing or order of events—such as Edwards et al. 1996, 1998). Aglaophyton and the appearance of photosynthetic indepen- Rhynia do have the extremely low stomatal dence, branching, and tracheids—in the evo- densities of 1.0 and 1.8 mmϪ2 respectively (Ed- lution of sporophyte independence within wards et al. 1998); however, that still amounts stem-group polysporangiophytes that pre- to 11 to 14 stomata per 1 mm of axial length, date the common ancestor of the living vas- whereas a density of 1 mmϪ2 in a cooksonioid cular plant ; that is exclusively axis of 150 ␮ thickness equates to 1 stoma per the of the fossil record. However, the 2 mm of axis. These isolated stomata are of general view has been that photosynthetic in- questionable utility (Edwards et al. 1998) and dependence and physiological continuity with indicate little potential for gas exchange over later vascular plants had already most of the life of the sporophyte. Hence, even been achieved prior to our oldest preserved if stomatal densities are similar, cooksonioids macrofossils, as has been directly stated or im- represent a special case difficult to equate plicitly required in paleobotanical studies of with larger Silurian and Devonian taxa. character evolution, physiology, and system- In bryopsid moss sporophytes, the tiered atics (Niklas et al. 1980; Raven 1984, 1993; Ed- apical growth may allow for differentiation of wards and Fanning 1985; Kenrick 1994, 2000; distal tissues and airspaces associated with Edwards et al. 1996; Kenrick and Crane 1997; the capsule before the intercalary elongation Bateman et al. 1998). The results of the current of the seta is complete (Crum 2001). However, study, in contrast, suggest that the establish- no such possibilities are available to branching ment of a physiologically independent spo- polysporangiophytes, which must have strict- rophyte generation has in fact been recorded ly apical growth. Hence, a cooksonioid with directly in the existing macrofossil record. stomata localized primarily to a sporangial No discrete and inviolate boundaries can be neck possessed no or almost no stomata for drawn between cooksonioids large enough to most of its growing life span: stomatal evi- possess tissue complexity and photosynthetic dence may well indicate that many cookson- capacity sufficient for functional indepen- ioid sporophytes were probably green, but not dence and those so small as to require pho- necessarily green enough to be photosynthet- tosynthetic dependence on a gametophyte; ically independent. however, several important transitions are likely to be recorded among described fossils. Discussion Several examples (e.g., Cooksonia cf. hemis- The Fossil Record of the Early Evolutionary His- phaerica [Edwards et al. 2004: Fig. 2]) possess tory of Polysporangiophytes. That the evolution axes more than 1 mm in diameter for which of a multicellular land plant sporophyte was there would be no reason to doubt photosyn- ancestrally an intercalary structure physiolog- thetic independence and for which rhizoma- ically dependent upon the gametophyte tous growth proves it. Other taxa (e.g., Uskiella throughout its ontogeny is overwhelmingly spargens [Shute & Edwards 1989] or Cooksonia 190 C. KEVIN BOYCE caledonica [Edwards 1970]) are large enough a possibility for the common ancestor of po- for photosynthetic independence, but none- lysporangiophytes or perhaps polysporan- theless possess a determinate growth pattern giophytes plus mosses (Kenrick 1994, 2000; suggesting they may still have been depen- Kenrick and Crane 1997). dent on a gametophyte for substrate interac- Regardless of whether any particular cook- tion. A variety of specimens in the 300–700 ␮ sonioid possessed genuine tracheids, their diameter range likely contributed significant- sporophyte branching places them in the larg- ly to their photosynthetic needs—as in many er polysporangiophyte clade (Kenrick and moss and sporophytes—but the Crane 1997) of which vascular plants are the possibility of actual photosynthetic indepen- only extant members. The smallest cookson- dence is increasingly remote with decreasing ioid sporophytes, highly unlikely to have been size, and particularly given the frequent pres- photosynthetically competent, suggest that ence of anatomical constraints such as hypo- gametophyte dominance is the primitive con- dermal tissues. And finally, near-complete nu- dition for the clade that includes the vascular tritional dependence upon a gametophyte plants and that isomorphic generations were would be the most parsimonious interpreta- derived within the group. This does not nec- tion for the smallest cooksonioids with axial essarily indicate the isomorphic rhyniophytes diameters as small as 30–70 ␮ (e.g., Cooksonia were a ‘‘dead end’’ (e.g., Gerrienne et al. 2006), pertoni, Salopella marcensis,andUskiella retic- because a switch from gametophyte to spo- ulata [Fanning et al. 1992] or Tortilicaulis offaeus rophyte dominance presumably would have and Salopella cf. marcensis [Edwards et al. involved an intermediate in which both gen- 1994]). erations were independent, albeit not neces- Alternation of Generations and Ancestral Ga- sarily isomorphic. metophytes. The recognition of perminerali- Validation of the ideas advanced here ulti- zations (Remy 1982; Remy et al. 1993; Kerp et mately must involve the search for a broader al. 2004; Taylor et al. 2005) and compressions diversity of gametophyte fossils among basal (Remy et al. 1980; Kenrick and Crane 1991) of polysporangiophytes, for which small cook- relatively large axial gametophytes with tis- sonioids suggest the need for a revised search sues as complex as in the corresponding spo- image. The isomorphic generations seen in lat- rophyte recast a century old debate over the er Rhynie Chert plants has led to the expec- origin of the land plant alternation of gener- tation that, if the oldest sporophytes looked ations. According to the homologous hypoth- like Cooksonia, then the oldest gametophytes esis (Church 1919), the ancestral sporophyte should also look like Cooksonia (Edwards 2000; and gametophyte generations were morpho- Kenrick 2000)—a solution unlikely if those logically and physiologically similar and have sporophytes are too small to be independent. since diverged. Alternatively, with the anti- If axial, the ancestral gametophytes likely thetic or intercalary hypothesis (Bower 1908), would have been either considerably larger the sporophyte represents a distinct innova- than the sporophytes or possessed external tion of multicellular complexity based upon elaborations of photosynthetic tissue as in the the delay of meiosis in an embryo retained by leafy bryophytes. Alternatively, a prostrate and dependent upon a larger gametophyte. and possibly thalloid gametophyte would With discovery of the Rhynie gametophytes, eliminate some of the structural support and Remy (1982) argued that gametophyte-domi- transport requirements of an erect axis. Thal- nant bryophytes and sporophyte-dominant loid candidate fossils are known (Tomescu tracheophytes were both descended from the and Rothwell 2006), although most of those isomorphic rhyniophytes. That view is no lon- with sporophyte attachment involve more-de- ger tenable given subsequent advances in un- rived taxa (Gensel et al. 2001) or at least spo- derstanding phylogeny (Mish- rophytes of larger size (Gerrienne et al. 2006) ler and Churchill 1984, 1985; Kenrick 1994, that likely are capable of photosynthetic in- 2000; Renzaglia et al. 2000); however, isomor- dependence (but see Fanning et al. 1992: Fig. phic generations continue to be considered as 54). HOW GREEN WAS COOKSONIA? 191

FIGURE 5. Phylogenetic distribution of axial diameters in basal polysporangiophyte fossils. Phylogeny from Ken- rick and Crane (1997).

Systematics and Taxonomy of Mid- such as the columella of Horneophyton,which Land Plants. Extremely small axial diameters likely would have to be a derived state rather suggestive of sporophyte dependence upon a than an ancestral one shared with a bryophyte gametophyte are rather dispersed across the sister group. Alternatively, if the currently fa- basal vascular plant phylogeny, so far as cur- vored topology is accepted, it must be under- rently understood (Fig. 5). This result is not stood that this implies that an independent simply a taxonomic artifact whereby the mis- sporophyte evolved multiple times—perhaps taken assignment of very small specimens has even among extant vascular plants, with spo- inflated the size ranges of taxa with larger ax- rophyte independence in the lycophytes and ial diameters; it is specifically the smallest fos- being separate events. Al- sils that have been included in the phyloge- though rejected in phylogenetic analyses netic analyses in some cases (Tortilicaulis of- based solely upon living plants (Mishler and faeus, Cooksonia pertoni [Kenrick and Crane Churchill 1985), multiple evolutions of spo- 1997]). This polyphyletic distribution may rophyte independence within the polyspor- highlight a lack of phylogenetic resolving angiophyte lineage are a necessary, albeit im- power and the usefulness of size as a character plicit, consequence of current phylogenetic to help resolve the tree topology. If small size, hypotheses involving sufficient fossil repre- as a proxy for photosynthetic dependence, sentation to address the issue (Kenrick and were considered ancestral and granted weight Crane 1997). as a character heavy enough to ensure a mono- That cooksonioid sporophytes possessed phyletic origin of sporophyte independence photosynthetic independence is rarely explic- within the polysporangiophytes, such a rear- itly stated, but is pervasively implicit in treat- rangement would question the current per- ments of early land plant taxonomy, system- ceived significance of other characteristics, atics, morphology, anatomy, ecology, and the 192 C. KEVIN BOYCE

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