ELSEVIER Review of Palaeobotany and Palynology 119 (2002) 143-159 Review of Palaeobotany ^Palynology www.elsevier.com/locate/revpalbo The ecology of Paleozoic ferns William A. DiMichele^*, Tom L. Phillips'' " Department of Paleohiology, NMNH Smithsonian Institution, Washington, DC 20560, USA '" Department of Plant Biology, University of Illinois, Urhana, IL 61801, USA Abstract Ferns or fern-like plants have been important elements of terrestrial vegetation since the Late Devonian. Rhacophyton, a fern-hke plant of the Late Devonian, appears to have been a colonizer of wet substrates, often forming large, nearly monotypic stands in peat-accumulating swamps. The earliest true ferns have been found in environments with high levels of disturbance, often fire, which suggest opportunistic, colonizing life histories, consistent with small, scrambling body plans. During the Early Carboniferous all major body plans and life histories of ferns appear, including scrambling ground cover, tree habit, and lianas. These ecological roles are distributed across several major lineages, including the Zygopteridales, Fihcales, and Marattiales, plus some fern-like groups of uncertain affinity, and disappear and reappear independently within these groups. Until the Stephanian, the later part of the Late Carboniferous, ferns largely were confined to secondary ecological roles: colonists, understory vegetation, small vines. Beginning in the latter part of the Westphalian and expanding dramatically in the Stephanian, marattialean tree ferns became the dominant trees of tropical lowland, wetland forests. This dominance continued locally into the Permian in wetter parts of the landscape. The Paleozoic ferns suffered major extinctions at several times, beginning in the Late Carboniferous. By the Permian, new lineages were appearing, some of which would persist into and become dominant vegetational components during the Mesozoic. Among these hneages virtually all of the hfe histories and body plans that characterized Paleozoic ferns would reappear independently, plus some new kinds of organization and ecology, emphasizing the great evolutionary flexibihty and responsiveness of fern-like construction and reproductive biology. ? 2002 Elsevier Science B.V. All rights reserved. Keywords: ferns; Paleozoic; ecology; paleoecology; evolution 1. Introduction Ferns are an ancient lineage of vascular plants. The first bone fide ferns appeared in the early Early Carboniferous, with fern-hke plants occur- * Corresponding author. Tel: +1-202-357-4480; Fax: +1-202-786-2832. E-mail addresses: dimichele.bill@nmnh.si.edu (W.A. DiMichele), tlphilli@life.uiuc.edu (T.L. Phillips). ring even earlier in the Late Devonian. As such, ferns are the last Class or body-plan clade of vas- cular plants to appear in the Devonian-Carbon- iferous radiation (DiMichele et al., 2001). Ferns are among the most recognizable groups to non- specialists. In detail, however, the taxonomic cir- cumscription of ferns is not such a simple task, especially during their early evolutionary history. Most of the characters shared by and considered to be uniquely characteristic of ferns are, in fact, primitive characteristics retained from their morphologically simple trimerophyte ancestors. Nearly aU ferns are homosporous and free-spor- 0034-6667/02/$ - see front matter ? 2002 Elsevier Science B.V. All rights reserved. PII: 80034-6667(01)00134-8 144 W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 ing, with consequent independent and free-living sporophyte and gametophyte life history phases, and have only primary bodies composed of large, compound (megaphyllous) leaves with circinate vernation, foliar borne sporangia, and adventi- tious roots. Most ferns have siphonostelic stems that produce stelar gaps in association with leaf- trace production; late Paleozoic small ferns were largely protostelic and thus lacked leaf gaps. This kind of reproduction and structure has been re- ferred to by Scheckler (1986b) as 'fern biology'. Many of the groups traditionally treated as ferns may be independent. Late Devonian derivatives of the trimerophytes (Galtier and Scott, 1985), shar- ing the basic characters of massive spore produc- tion, clonal reproduction, and large leaves with stem-like developmental aspects (Rothwell, 1999). As such, the concept of 'fern' is an organizational grade based on common morphological attrib- utes. In this essay, we consider the ecological history of Paleozoic ferns. In so doing, we have accepted the broad definition of 'fern biology' referred to above. The ferns have an extensive fossil record, which includes excellent examples of both anato- my and gross morphology. However, nearly all fossils are simply fragmentary remains, preserving only a portion of the plant body, often without clear connection between reproductive and vege- tative organs. Furthermore, the rarity of such forms in adpression preservation suggests a strong preservational bias against small, surface-creeping growth habits, unless the plants formed extensive clones; coal balls are an exception because they preserve plants in situ. Structural preservation has played an inordinately important role in decipher- ing the biology of many fossil ferns, given its rel- ative rarity, because it reveals subtle details of growth and reproduction. The fern fossil record, particularly from the Paleozoic and Mesozoic, shares a common taphonomic megabias with oth- er fossil floras of these times - plants from basinal wetlands are by far the most likely to be preserved in the fossil record, screening from us much evo- lutionary innovation that may have taken place in the more demanding, environmentally extreme areas of the ancient extrabasinal lowlands and basin-margin uplands. The ecology of fossil ferns can be elusive, espe- cially at the species level. The bulk of the litera- ture on fossil ferns is concerned with systematics and morphology, rather than the environmental context needed to infer many aspects of paleo- ecology. Ecology can be deduced from some as- pects of functional morphology, although due caution must be exercised. An understanding of fern paleoecology is derived largely from floristic or diversity studies focused on a larger spectrum of plant groups (e.g., Scott, 1978; Pfeflerkorn and Thomson, 1982; Lesnikowska, 1989; Pryor, 1993; Lyons et al., 1997). Studies of modern ferns in- clude more information and, while most focus on systematics and morphology, provide more com- plete understanding of growth architecture and the timing of various growth and reproductive events. Ecological patterns also have been the ex- plicit focus of some studies (e.g.. Page, 1979) and appear as observations in many systematics pa- pers. In addition, the modern record informs us of the complex chemical controls on many aspects of homosporous fern reproduction not accessible to studies of fossils. Our examination will emphasize, for the most part, ecological patterns at the species level, with a focus on growth architecture, habitat preferen- ces, and strategies permitting successful growth and reproduction. Where appropriate, we will consider the dynamics of fern-dominated com- munities. We will not consider the role of ferns in the biostratigraphy of Paleozoic terrestrial rocks, although they are important in this ca- pacity (e.g., Zodrow and Cleal, 1985; Wagner and Winkler Prins, 1991; Cleal, 1997). There are several generalities that can be drawn from this review. Ferns have ventured into most ecological roles, from ground cover, to epiphytes, to forest trees, have grown in most kinds of habitats, from fire swept, to swampy, to xeric, and have ex- ploited resources with a range of life-history strat- egies, from opportunists to resource accumula- tors. These roles have recurred throughout geological time, evolving independently in many different lineages. There are very few extinct fern ecologies, although there may be some when ex- amined in terms of the scale at which a particular Ufe form dominates the landscape. W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 145 2. The early ferns The earliest fern or fern-like plant is Ellesmeris sphenopteroides (Hill et al., 1997) from the Late Devonian (Frasnian) of the high Arctic. It is zy- gopterid-like with laminate pinnules; however, its ecology is not well understood. Better known eco- logically is the related Rhacophyton ceratangium, known from the Late Devonian and earliest Early Carboniferous (Andrews and Phillips, 1968; Cor- net et al., 1976). We do not include the Cladox- ylales in this discussion because of the confusion this introduces regarding the nature of true ferns. Rhacophyton was a shrub or subtree that lacked laminate foliage but bore some determinate lateral branches that terminated in a dense mass of di- chotomies, forming a light intercepting surface. Chaloner (1999) proposed that the development of such laminate foliage may be related to the global decline of CO2 in the Late Devonian (Berner, 1998), favoring morphologies more con- ducive to CO2 diffusion. Rhacophyton had typical fern biology: massive production of isospores, possibly clonal growth (Scheckler, 1986b), and frond-like branch systems as the major organs of the plant. Rhacophyton appears to have been the sole to overwhelmingly dominant plant in swampy, coastal lowland environments of the southeastern United States, where its organic remains formed thin coals. The plant was not confined to this habitat, however, but also was an element of low diversity, mixed communities on better drained substrates (Scheckler, 1986a,b). During the Late Devonian, species diversity in the subtropics, from which the plant is known, was low providing only a small number of taxa for landscape development, which possibly permitted a species to play a variety of eco- logical roles. This was a time of origin of the major body plans of vascular plants and the ecological centroids that would characterize these major groups during the Carboniferous when they were still being sorted out (Di- Michele and Bateman, 1996; DiMichele et al., 2001). A great variety of plants recognizable as ferns by their gross morphology made their first ap- pearance in the Early Carboniferous. They belong to three major groups, the early filicaleans, the zygopterids, an extinct group, and the marattia- leans. Almost ah of these plants were homospo- rous, small, prostrate, clonal forms often de- scribed as 'sprawling' or 'rampant' (Phillips, 1974; Galtier and Holmes, 1982; Gahier and Phillips, 1996; Scott and Galtier, 1996), except the Marattiales. The known early marattialean stems indicate that they were arborescent forms (Goodlet, 1957; Remy and Remy, 1977; DiMi- chele and Phillips, 1977) of relatively small stature compared to later Carboniferous species. Upright, possibly small tree stature has been described for the Visean age Australoclepsis australis, made pos- sible by a false stem made up of many smaller stems (Sahni, 1928). The small ferns appear to have occupied a wide range of physical conditions where they most often grew as opportunists in disturbed environments (Scott and Galtier, 1996). Many ferns, such as the filicalean Botryo- pteris antiqua, were common and cosmopolitan, and are well known from anatomical preservation in permineralized peats (Rex, 1986; Scott and Galtier, 1996). The zygopterid, Clepsydropsis, seems to have preferred alluvial and lagoonal set- tings where water tables were high but peat accu- mulation was minimal (Scott et al., 1984; Scott and Galtier, 1985). At the other extreme from these wetter sites, ferns of the later Early Carbon- iferous appear to have been well established in harsh environments, frequently disturbed and often fire-prone, where they are anatomically pre- served as charcoal or occur in regular association with charcoal. Prominent in these settings were the zygopterids Diplolabis and Metaclepsydropsis (Scott and Rex, 1987; Rex and Scott, 1987). Many of these fire-prone habitats are associated with volcanic activity and the nature and quality of the substrates may have been very patchy. Scott and Galtier (1985) suggested such fire-swept environments were a major selective force in the early history of ferns, and helped hone op- portunistic life histories. Certainly, ferns remain important colonizers of landscapes disturbed by fires and volcanic activity, and often are among the first plants to reappear in these kinds of hab- itats following catastrophic disturbance (Burn- ham and Spicer, 1986; Retallack, 1992). Within 146 W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 Early Carboniferous, subtropical habitats, from which these patterns are known, fern abundances were highly variable, strongly suggesting patchy distributions. Similarly, the correlation between specific habitats and fern floras is weak because of the generally low abundance of ferns, al- though the most consistently high abundances and co-occurrences are with pteridosperms (seed ferns) in wet flood-plain environments (Scott et al., 1984). 3. Late Carboniferous and Permian ferns 3.1. Small ferns 3.1.1. Small-fern diversification The small ferns underwent three major radia- tions (Rothwell, 1987). The first, near the Devon- ian-Lower Carboniferous boundary generated a number of families that did not survive the Paleo- zoic. The oldest families were in the Zygopteri- dales, with architecture, anatomy and reproduc- tive organs distinct from those of the filicalean ferns. Most of the other forms are clearly identi- fiable as filicalean, including Botryopteridaceae, Psalixochlaenaceae, Anachoropteridaceae, and Tedeleaceae. A second filicalean radiation took place in the Permian, and generated a number of families that would rise to prominence in the Mesozoic, all apparently derived from the earlier filicalean forms. Many of the features of modern ferns, now considered advanced, evolved within the primitive filicalean families, and may have evolved more than once, independently in several of the lineages (Galtier and Phillips, 1996). It ap- pears fairly certain that laminate foliage evolved independently in a number of fern groups, al- though the stem-leaf appendicular relationship is plesiomorphic (Phillips, 1974). As a consequence of the basic flexibility of their life history and simple growth architecture, Paleozoic ferns be- came members of plant communities in a broad array of habitats. Appreciation of this is some- what limited by the nature of Lower Carbonifer- ous exposures, but filicalean and zygopterid ferns from the Upper Carboniferous, clearly manifest a vast array of ecological roles. 3.1.2. Small-fern patterns of occurrence Ferns are rare in local community analyses based on compression assemblages throughout the Permo-Carboniferous, representing clastic flood-basin habitats. In the Westphalian B of Yorkshire (Scott, 1977, 1978, 1979) the few filica- lean species encountered occur at 1-10% cover in low diversity and only in flood-plain habitats, rec- ognized as laminated mudstone with common rooted horizons; marattialean ferns are an insig- nificant part of lowland wetlands at this time. In flood-plains, rare ferns are found in monospecific stands, probably clones (Scott, 1978; Scott and Galtier, 1985). Community analyses of younger Westphalian D compression floras also reveal low filicalean fern diversities, similar to those found by Scott (Lamboy and Lesnikowska, 1988; DiMichele et al., 1991), although marattia- lean tree ferns are abundant. The low diversity of small ferns in community analyses of compression floras may be reflective of several factors. Of most importance is the appar- ent patchy distribution of small ferns, which, combined with small biomass and the lack of or- gan abscission in most species, severely restricts the input of tissues and organs to environments of burial. Also important is the sampling scale, generally quite restricted in most analyses of local communities. Limited sample size and coverage is mitigated in fossil assemblages to some extent; plant remains of compression floras were gener- ally transported from the environment of growth to the environment of deposition, even if only a short distance. Thus, intrahabitat transport of de- bris can reduce the impact of restricted sampling by homogenization of the flora, to some extent, but only for those plants that shed leaves and other parts. Overall, therefore, the interaction of sampling scale and preservational bias tends to reduce apparent fern abundance and local, intra- community species richness. In contrast to analyses carried out at small spa- tial scales on essentially local floras is the al- lochthonous Mazon Creek flora of Westphalian D age. The Mazon Creek flora, which is collected from brackish to marine shales, is drawn from a large terrestrial source area, and therefore is not a picture of community diversity, but rather of the W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 147 diversity in the regional species pool. In addition, Mazon Creek may be the most heavily collected and best known Pennsylvanian age flora from western Euramerica. According to the analysis of Pfefferkorn (1979), ferns are the most diverse group of plants in this flora, comprising 37 of the 96 described 'whole plant' species. Twelve of these species are marattialean ferns, which had become diverse and abundant by the late Westphalian D, and the remaining 25 are small ferns, known mainly from their reproductive organs. This con- trast suggests that small ferns were diverse at the regional spatial scale, but perhaps quite patchy and localized in their distributions within a re- gion, rarely forming an abundant grass-like ground cover over broad areas. Studies of peat-substrate floras, preserved in coal balls, provide a more compelling picture of small-fern ecology. Because coal balls are permin- eralized peat stages of coal, they capture both tree litter and groundcover on the floor of the swamp or mire. In some of the oldest Upper Carbonifer- ous coal-ball floras, from the Westphalian A of Britain and western Europe, ferns are a common component. The Bouxharmont Seam of Belgium (Holmes and Fairon-Demaret, 1984), for example, is rich in ferns; 17 species have been identified, occurring on a frequency rather than biomass ba- sis in 25% of the 500 coal balls examined, ranking behind arborescent lycopsids and sphenopsids, and above pteridosperms. Nearly all these ferns are groundcover or facultative climbers/sprawlers. Quantitative analyses of coal balls from the Union and Bouxharmont seams (Phillips et al., 1985) indicate that small ferns were minor bio- mass contributors, despite their species diversity, accounting for less than 10% of total peat bio- mass. A similar pattern is found in coal beds throughout the Pennsylvanian of North America and Europe. Small-fern diversity in the coal-ball analyses of the Westphalian D coals of the United States is nine species that, on average, account for less than 2% of the biomass in any given coal seam (Phillips et al., 1985). 3.1.3. Small-fern growth habits and ecologies Small ferns of the late Paleozoic had evolved a remarkable array of growth architectures, paral- leling those seen in modern ferns. These growth forms are summarized by Galtier and Holmes (1982). They fall into four basic categories. (1) Species with upright growth habits, often un- branched. Included are some zygopterids, most species of Tubicaulis (an anachoropterid), some species of Ankyropteris {A. hendricksii, Read, 1938) of the Tedeleaceae, and the three species of Grammatopteris (Sahni, 1932; Tidweh and Ro- zefelds, 1990). (2) Rampant forms without a clear relationship between phyllotaxy and stem dichot- omy. Included are a number of zygopterids, in- cluding the early ferns Diplolabis and Metaclepsy- dropsis, as well as Zygopteris, Psalixochlaena, and Botryopteris. (3) Forms with axillary branching included Psalixochlaena, Ankyropteris, and some species of the anachoropterid Tubicaulis. (4) Forms with cauline units originating from buds on fronds included many species of Botryopteris, Anachoropteris, and Psalixochlaena. These different growth architectures permitted small ferns to acquire a variety of growth habits and occupy a wide range of ecological roles. Most species likely formed surface creeping ground cov- er, especially those with rampant habit or with axillary branching. This includes most species of the Zygopteridaceae, a family extending from the Late Devonian into the Permian, including the genera Clepsydropsis, Metaclepsydropsis, Diplola- bis, Zygopteris, and Nemejcopteris (Dennis, 1974; Phillips, 1974; Barthel, 1968) (Fig. 1). Many spe- cies of Botryopteris and Anachoropteris may have been much like modern 'walking ferns' that pro- duce stem buds on fronds enabling them to spread rapidly across open substrates (Phillips, 1974; Trivett and Rothweh, 1988). In the case of Psalixochlaena, its prostrate stem may have been subterranean, given that it can occur in ex- ceflent preservation (Holmes, 1977) in otherwise heavily rotted root peats, suggesting penetration of the substrate. Assemblages of small ferns, minimally fragmented and apparently in place, can be found commonly in coal balls (Plate I, 1), occupying what appear to be exposure surfaces in the peat (Phillips, 1974). Such assemblages often are mixed and their commoness indicates a convergent cross-species ecological strategy among the rampant forms, aimed at exploitation 148 W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 149 of open areas, possibly after some kind of distur- bance. Upright habit permitted the evolution of small trees or shrubs. This habit has been suggested for Zygopteris primaria (Sahni, 1931a). Tidwell and Rozefelds (1990) suggest that some Grammatopte- ris species may have been upright. Climbing habit has been suggested for many species. A liana growth form has been suggested for an Anachoropteris species, based on coal balls of Late Pennsylvanian age (Trivett and Rothwell, 1988). This species has latent croziers that have been found to replace basal pinnae on fronds oth- erwise fully developed. Facultative climbing habit has been suggested for Ankyropteris brongnartii (Stenzel, 1889; Sahni, 1935; Mickle, 1980, 1984; RoBler, 2000), of the Tedeleaceae (Fig. 1) and for Botryopteris cratis (Phillips, 1974; Millay and Taylor, 1980) of the Botryopteridaceae based on their occurrences both as prostrate stems and em- bedded in root mantles of Psaronius (Plate I, 2, 3) from a number of Late Carboniferous and Per- mian localities. Epiphytic ferns may have been common, but this habit is possibly the most difficult to docu- ment. An epiphytic habit has been suggested for Botryopteris forensis (Rothwell, 1991). This plant was first suggested as an epiphyte by Mamay and Andrews (1950) based on its growth architecture and association with Psaronius root mantles (Fig. 1). Association of small-fern stems of the genus Tubicaulis with tree-fern root mantles has led several other authors to suggest an epiphytic habit for T. berthieri (Bertrand, 1909; Bertrand and Bertrand, 1911) and Tubicaulis sp. (Sahni, 1931b, 1935; RoBler, 2000) of Permian age, and for the Pennsylvanian species T. scandens (Ma- may, 1952), which, as its name indicates, had long internodes and a slender stem. RoBler (2000) has found a close association of Anachor- opteris foliage with Tubicaulis stems in Permian material from Chemnitz embedded within Psaro- nius root mantles, an organ association known for some other, non-epiphytic, species of Tubicaulis. RoBler (2000) also has identified a small stem attributable to Grammatopteris (Kidston and Gwynne-Vaughan, 1907; Beck, 1920; Miller, 1971), embedded with the root mantles of Per- mian-aged Psaronius stems; this association sug- gests a growth habit quite different from that for other species of this genus, which, as noted above, may have been small tree ferns (Tidwell and Ro- zefelds, 1990). 3.1.4. The association of small ferns with fire Small-fern debris in coal balls is commonly pre- served as charcoal (Plate I, 4). In such instances, the remains of stems, foliage, reproductive organs and roots often are fragmentary and not clearly associated with a diagnostic site of growth. In keeping with other ancient and modern observa- tions, filicalean and zygopterid ferns of the late Paleozoic appear to have grown in habitats that were periodically disturbed, and fire is and was one of the major disturbance agents in those hab- itats. Disproportionate fusain preservation, by itself, should not be taken to indicate growth in fire- prone habitats, however. Given that most small filicaleans and zygopterids did not readily disinte- grate into separate, easily transportable organs, that they were often ground cover, sheltered from destructive winds, and that their populations were patchy in time and space, preservation of plants should have been much rarer than was characteristic of canopy trees. This observation is supported by modern actualistic studies (Scheihing, 1980), wherein ground cover was found to be disproportionately rare following ma- jor storm events that created substantial fresh de- bris. Fire, on the other hand, will kill and frag- ment these small, clonal plants. Charcoal is light, Fig. 1. Late Pennsylvanian (Stephanian) tropical coal-swamp scene in a Psaronim tree-fern-dominated area with exposed peat, some charred debris, and abundant fern ground cover, especially in light gaps. Setting based on coal-ball observations in the Cal- houn Coal, Berryville, Illinois. At right: Ankyropteris brongnartii climbing on the outer root mantle of Psaronius blicklei tree-fern trunk. At trunk base, Botryopteris forensis with some globose fertile pinnae on otherwise laminate fronds. At left: large stand of Zygopteris herryvillensis with erect fronds and perpendicular pinnae. Lower left: charred Tubicaulis rhizome. 150 W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 o;-; >! ii>^- ^?^-i!? .pi ^^- say :*^^ & - ?*^ >.iS^. W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 151 highly transportable, and resistant to degradation. Consequently, the common fusinization of small ferns may simply reflect a strong taphonomic bias in the nature of litter input into the potential fos- sil record - if burned and fusinized the likelihood of preservation and detection increases signifi- cantly. 3.2. Marattialean tree ferns 3.2.1. Marattialean diversification The evolutionary history of the Marattiales has been reviewed by several authors in the past quar- ter century (Stidd, 1974; Hill and Camus, 1986; Millay, 1997). In broad terms, the group does not appear until the Namurian, in the latest Early Carboniferous (Goodlet, 1957; Remy and Remy, 1977; Gerrienne et al., 1999). The geographical origin appears to be tropical and Euramerican, based on the first occurrences and the pattern of later global radiation in the Stephanian. The near- est relatives or likely ancestors are unclear. Mar- attialean ferns have typical fern biology - mega- phyllous leaves, siphonostelic stems, adventitous roots only, homosporous reproduction, abaxially foliar borne sporangia, and prolific production of isospores. The Marattiales are eusporangiate, however, and do not seem to be allied closely with other common Paleozoic ferns. The phyloge- netic linkages between the dominant Paleozoic forms and those typical of the Mesozoic, persist- ing until today, are not agreed upon either. Both Stidd (1974) and Delevoryas et al. (1992) suggest descent of the two groups from common, largely unrecognized Paleozoic ancestors, rather than one from the other; Radstockia is posited as a likely member of the ancestral plexus and may have been an element of extrabasinal floras, occurring as it does rarely in the Mazon Creek flora and in other clastic adpression assemblages. In contrast. Hill (1987) argues that there are sufficient similar- ities in a number of Paleozoic species to indicate derivation of the extant lineages from late Paleo- zoic precursors. On the basis of adpression foliage and both adpressed and structurally preserved reproductive structures, marattialean species diversity literally exploded during the Stephanian (Late Pennsylva- nian) (Boureau and Doubinger, 1975; Miflay, 1997). Prior to that time, tree ferns were an in- creasingly important part of tropical floras, begin- ning their quantitative rise to prominence in the wetlands during the Westphalian B, based on the spore record and during the early Westphalian D, based on the record of macrofossils (Pfefferkorn and Thomson, 1982; Phillips et al., 1985). By the late Westphalian D, a majority of adpression flo- ras, likely from wet flood-plain habitats, were dominated by marattialean tree ferns (Pfefferkorn and Thomson, 1982); in contemporaneous peat swamps, tree ferns had become common, and dominated some local assemblages within these edaphically restricted environments (Phillips and DiMichele, 1981; DiMichele and Phillips, 1988). However, they remained at about 10-20% of the peat biomass when averaged across the peat- swamp landscape (whole seam basis). Near the Westphalian-Stephanian (approximately equals the Middle-Late Pennsylvanian) boundary, dra- matic changes in tropical vegetation occurred, es- Plate 1. Transverse cut through peat reveahng a Zygopteris horizon with three rhizomes (circled by dotted lines) crossing each other. 1.8 X. University of Illinois Coal Ball Specimen 38896, Herrin (No. 6) Coal, Middle Pennsylvanian, Shawneetown, Illinois. Cross section of part of the upper stem of Psaronius (upper right) with inner root mantle (ir) and three adjacent shoots of Ankyropteris alongside the trunk (arrowheads). 2 X. University of Illinois Coal Ball Specimen 7406B, Herrin (No. 6) Coal, Middle Pennsylvanian, Sahara Coal Company Mine No. 6, Illinois. Cross section of about half of a P.saronim trunk with irregular inner root mantle (ir) and adjacent Ankyropteris stem (s) and petiole (p). 1.8 X. University of Illinois Coal Ball 22686B, Cross section of Tuhicaulis stem (s) with petioles distally exhibiting Anachoropteris involuta-typs xylary configurations. The in situ specimen terminates in upper levels in charred remains (arrowheads), consistent with loss in ground fire. Long arrow points to stele of stem. 2.1 X. University of Illinois Coal Ball 524762, Middle Pennsylvanian, Urbandale Mine, Iowa. 152 W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 Plate II. 1. Cross section of stem of Psaronius hlicklei with small distelic stem (s), thick inner root mantle (ir) and part of the outer root mantle (or) of large free roots. 0.4 X. USNM Specimen 458422, Calhoun Coal, Upper Pennsylvanian, Berryville, Illinois. 2. Coalified compression specimen of Pecopteris cf. cyathea, foliage of Psaronius. 2.5 X. Upper Pennsylvanian, Texas, USNM Locality Number 39997. 3. Coalified compression of Pecopteris puertollanensis, fohage of Psaronius. 1.4 X. Upper Pennsylvanian, Texas, USNM Locahty Number 39992. W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 153 pecially in the western parts of Euramerica, thought to be induced by major changes in cH- mate (Philhps et al., 1974; Phihips and Peppers, 1984; Frakes et al., 1992; DiMichele and Phillips, 1996). Fohowing these disruptions, tree ferns rose to prominence, quantitatively dominating many lowland, wetland habitats and also diversifying greatly. The exact number of species is difficult to determine, despite the many described forms. The genus Pecopteris appears to taxonomically oversplit, possibly enormously, but in a complex way reflecting fragmentary preservation, complex intrafrond morphological differences, and region- al taxonomic differences, both real and resulting from historically different practices in different parts of the world. 3.2.2. Marattialean growth habits The classic image of a Paleozoic marattialean fern is the reconstruction in Morgan (1959), which has been widely reproduced: a straight- growing, arboreous plant several to perhaps 10 m or more in height, its primary stem mantled by adventitious roots, topped by a crown of large, graceful, compound fronds. The largest reported basal diameter is 1 m or more (Willard and Phil- lips, 1993) from Late Pennsylvanian deposits of Illinois in the USA. In Permian deposits of Chem- nitz in Germany, RoBler (1995) estimates stem diameters up to 1.5 m when a correction is made for preservational distortion. The stems of these plants are classified as Psaronius, if pre- served anatomically (Plate II, 1), a name that has come to be used as shorthand for the entire plant, or as several other genera if preserved as adpression fossils (Megaphyton, Caulopteris, Arti- sophyton, depending on arrangement and nature of leaf scars, Pfefferkorn, 1976); foHage is gener- ally of the Pecopteris-iype (Plate II, 2, 3), and, if fertile, most often bears radially symmetrical syn- angia classified as Scolecopteris or several other genera (Millay, 1979). This was the typical mar- attialean growth form of the late Middle Pennsyl- vanian and Late Pennsylvanian tropical lowlands. It persisted through the Permian (e.g., RoBler, 2000) and into the Triassic, where it was finally replaced by forms typical of modern groups (Del- evoryas et al., 1992), with bilaterally symmetrical synangia, foreshortened stems, and no root man- tle. The earliest marattialeans appear to have dif- fered considerably from this growth form, based on the limited evidence at hand (Pfefferkorn, 1976; Remy and Remy, 1977; DiMichele and Phillips, 1977). These forms, which occur from the latest Mississippian into the Early Pennsylva- nian, are anatomically much simpler than later forms, with monocyclic dictyosteles instead of the polycyclic dictyosteles of younger forms. Although arborescent, given the lengths and di- mensions of the stems, they appear to have had very limited root mantle development. Fronds were borne distichously, meaning that in compres- sion, the stems would be classified as Megaphyton, and due to the lack of associated Pecopteris re- mains, may have been of some other, perhaps sphenopterid form. Given the totality of the evi- dence, Millay (1997) suggested that these early forms should be placed in a distinct genus rather than in Psaronius. Stems with polycyclic organization, probably of tree habit, are known from the Westphalian A (Early Pennsylvanian equivalent) of England (Scott, 1920), and correspond to the rise in im- portance of Pecopteris and Scolecopteris. Lesni- kowska (1989), in a detailed study of the mor- phology of marattialeans in coal-ball deposits, determined that a number of Middle Pennsylva- nian marattialeans were of considerably smaller stature than that portrayed in Morgan (1959), generally with small diameter stems and thin root mantles. She even described one species that lacked a root mantle altogether and had a sprawHng growth form. Mickle (1984) hinted at the existence of a similar growth form in the Late Pennsylvanian, based on a single petrified specimen completely lacking a root mantle, but could not unequivocally rule out the possibility of it being a developmentally young plant. Climb- ing and epiphytic growth habits have not been suggested for any Paleozoic marattialeans. 3.2.3. Paleozoic marattialean ecology Early marattialeans, those with 'monocyclic', simple stem anatomy, frequently are preserved as sandstone casts, bearing little morphological 154 W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 or contextual evidence of ecological preference. The form of preservation suggests growth near streams in wet habitats. Possibly the best docu- mented of these early forms, in terms of its ecol- ogy, is Psaronius simplicicaulis from the Early Pennsylvanian of Illinois (DiMichele and Phillips, 1977). This plant evidently was a tree fern of small stature. Its remains occur in dark, pyritic, organic shales that represent the final phases of clastic, mud fill in narrow, steep-sided channels cut into limestone bedrock. Most of the channel fill is light gray siltstone bearing a distinctive 'ex- trabasinal' flora (Leary, 1981), probably represen- tative of plants growing along the margins of the channels while water was actively flowing. The tree ferns occur in association with lycopsid trees in what seems to have been a stagnant-water, swamp assemblage that formed as channels were cut off" or drowned. Thus, the earhest known forms seem to be associated with wet habitats, but possibly within broader, seasonally dry or well-drained landscapes. Marattialeans are notably rare in clastic adpres- sion assemblages from the Westphalian A and B (Early and early Middle Pennsylvanian) (e.g., Scott, 1977, 1978). In the Westphahan C and D (Middle Pennsylvanian) they colonized the wet lowlands, primarily in clastic-substrate environ- ments, becoming important components of ad- pression floras, rising to biomass dominance in many (Pfeflferkorn and Thomson, 1982). The subtleties of physical control on these plants are not particularly clear, due to transport and frag- mentary preservation. Stephanian tree ferns occu- pied a wide range of flood-basin habitats from moderately well-drained soils to swampy sites, continuing the expansion in diversity and ecolog- ical dominance that started in the late Middle Pennsylvanian. Most of the described adpression species of Pecopteris (or its segregate genera, Lo- batopteris and Polymorphopteris) are from the Ste- phanian. The ecologies of these individual species are, for the most part, unknown. What can be said is that many species of Stephanian tree-fern foliage can co-occur at a single, environmentally homogeneous collecting site, that species richness tends to be higher in non-swamp flood-basin de- posits, those that may have been more aerated or periodically dry, than in stagnant-water swamps (DiMichele and Mamay, 1996; Barthel and Weiss, 1997), and that maximal tree size was at- tained during the Stephanian and Early Permian based on in situ stumps and the diameters of per- mineralized stems (e.g., Cross, 1952; Mickle, 1984; Lesnikowska, 1989; RoBler, 2000). Personal observations suggest that there are species differ- ences in habitat preferences of many pecopterid species, something also alluded to by Mickle (1984); these have yet to be documented in detail. The expansion of tree ferns into peat substrate floras was gradual and by the late Middle Penn- sylvanian, such ferns were an important and wide- spread component of these habitats (Phillips et al., 1985). Quantitative study of coal-bah floras has revealed some important aspects of tree-fern ecology in peat swamps. The following points are taken from data and discussion in Phillips and DiMichele (1981) and DiMichele and Phillips (1988), Willard (1993) and Phillips and DiMichele (1998), studies of late Middle Pennsylvanian coals. Tree ferns appear to have been excluded during the Middle Pennsylvanian from the wettest habitats in peat swamps, those inferred to have long periods of standing water, dominated by spe- cies of the lycopsid tree Lepidophloios, which gen- erally lack all vestiges of ground cover as well. This is not surprising, considering the free living, terrestrial gametophyte phase of the marattialean life history. They are components of virtually all other assemblages, at about 10-20% of aerial bio- mass on average, varying independently of the dominant elements. Most species of these late Middle Pennsylvanian tree ferns appear to have been opportunists, exploiting disturbance. Indi- vidual species do not have diagnostically specific distributions with regard to habitat markers such as charcoal, clastic partings, or clastic enrichment of the coal, markers that do correlate strongly with species from other taxonomic groups, such as lycopsids and pteridosperms. In general, early Middle Pennsylvanian tree ferns in coal swamps were of relatively small stature compared to those that would dominate Late Pennsylvanian swamps. Lesnikowska (1989) compiled data on organ di- ameters and discovered that only in the latest coals of the Middle Pennsylvanian do root diam- W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 155 eters appear that rival those found in the Late Pennsylvanian. During the transition from the Middle to the Late Pennsylvanian, extinctions of lycopsid trees began, spreading from west to east across the Euramerican-Cathaysian tropics (Phillips et al., 1985). This extinction wave did not reach the rain forest areas of Cathaysia, where typically Middle Pennsylvanian vegetation persisted into the Late Permian (Guo, 1990). The disruption of swamp vegetation was accompanied by extinction of nearly two-thirds of the species, including most of the trees (DiMichele and Phillips, 1996). In the resulting Late Pennsylvanian coal swamps, tree ferns appeared as the dominant elements, includ- ing trees of large stature, but representing an al- most complete turnover in tree-fern species (Les- nikowska, 1989). In Late Pennsylvanian coal swamps of the Illinois Basin, marattialean tree ferns account for 60% to over 80% of peat bio- mass (PhilHps et al., 1985). More detailed ecolog- ical analyses of these swamp assemblages (Pryor, 1993; Willard and Phillips, 1993; DiMichele and Phillips, 1996) suggest that tree ferns occurred in most mire subhabitats, dominating many, espe- cially on thick peats with little mineral matter. Edaphic variation in the swamps appears in the distribution of subdominant elements such as me- duUosans, cordaites, and sigillarian lycopsids. Pryor (1993) and Grady and Eble (1990) have described patterns of species succession, corre- sponding to changes in the amount of mineral matter and evidence of peat decay. In general, plants other than tree ferns dominate those as- semblages associated with the base of the coal bed or with mineral bands in the coal, tree ferns rising to importance in the thicker parts of the seam. The era of marattialean importance lasted well over 10 Myr, beginning in earnest at the end of the Middle Pennsylvanian and continuing into the Permian. For most of this time marattialean tree ferns were part of floras that would be categorized broadly as 'wetland', rich in pteridosperms and lycopsids, associated with organic-rich deposits of various sorts, and generally connected evolutio- narily to the floras of the Carboniferous tropical lowlands (Fig. 1). During the Permo-Carboniferous transition new floras began to appear that were dominated by a variety of xeromorphic seed plants, such as conifers and callipterids. These new floras shared few species with those of the primordial tropical wetlands and gradually became predominant in the tropical lowlands as climatic seasonality in- creased (Knoll, 1984; Broutin et al., 1990; DiMi- chele and Aronson, 1992). The marattialean tree ferns were one of the few groups with species in tropical wetlands that also were locally abundant in the newly emerging lowland vegetation, which appears to have grown under seasonally dry con- ditions. Studies of the floral transition in north- central Texas (DiMichele and Mamay, 1996) in- dicate that tree ferns were persistent elements in the newly appearing vegetation, probably in wet- ter areas, but in association with conifers and other plants that would dominate the Permian landscapes. They persist, and even dominate sites on occasion (Mamay, 1968) wefl into the later part of the Early Permian in the western US, ul- timately disappearing as conditions become very dry in that part of the world. Their ability to make this ecological jump from one dominant flora to the other may reflect their fundamentally opportunistic life histories and flexible body plans, the same characteristics that contributed to their ascendency following the Middle-Late Pennsylvanian extinctions. Such a life history pre- disposes the plants to the formation of ecologi- cally evolutionary isolates and encourages specia- tion in the course of opportunistic resource exploitation. 4. Discussion The Paleozoic fern radiation gave rise not only to most of the major taxonomic groups, but also saw the evolution of nearly all the basic body plans ever to appear within this clade. Impor- tantly, however, these growth habits evolved across the full spectrum of the existing groups. Trees appeared in both the Marattiales and Zy- gopteridales, epiphytes, vines and sprawling ground cover in the Filicales and Zygopteridales, and upright shrubby plants and subtrees in the 156 W.A. DiMichele, T.L. Phillips I Review of Palaeohotany and Palynology 119 (2002) 143-159 Marattiales and Filicales. Among the filicalean groups, the variety of anatomy and architectures was greater than that seen after the Paleozoic, when a second major radiation of this group took place (Rothwell, 1987). Virtually all the Paleozoic groups were replaced in the Mesozoic, when the Filicales rose to prom- inence. In this instance we are including the Os- mundaceae in the Filicales. Filicaleans included many species with surface ground cover growth habits, many of which have persisted until today. Modern tree ferns are entirely filicalean in affin- ities. And, false stems can be found in modern Hemitelia as well as in the fossil filicalean Temp- sky a (Andrews and Kern, 1947). Filicaleans also are epiphytes and vines. In addition, aquatic ferns of the Hydropteridales, a group of filicalean affin- ity, appeared in the Mesozoic, adding a new di- mension to fern ecology (Rothwell and Stockey, 1994). Thus, many of the life habits found in Pa- leozoic ferns re-evolved in the Mesozoic, although on a narrower phylogenetic base than earlier. Within the confines of the diversity of body plans. Paleozoic ferns occupied a wide range of habitats and played many ecological roles. Early forms included both opportunists, capable of ex- ploiting disturbed and possibly burnt-over land- scapes (Scott and Galtier, 1985), and more typical ground cover in a variety of settings. By the end of the Middle Pennsylvanian, tree ferns had be- come important dominants in wetlands (Phillips and Peppers, 1984), forming what may have been the most extensive fern-dominated land- scapes of the Phanerozoic. A remaining question is the role of ferns as ground cover. Clearly, there are places today where fern thickets can cover broad areas. However, the evidence available from Paleozoic rocks does not reveal extensive stands of ferns analogous to the grasslands of to- day. Such a ground cover role has been postu- lated for Mesozoic filicaleans (Coe et al., 1987; Wing and Tiflfney, 1987), based on inferences about dinosaur feeding habits rather than direct evidence. In conclusion, fern biology, in its morphologi- cal simplicity, appears to have permitted the ferns to remain evolutionarily flexible, by not placing strong constraints on the direction of evolution. As a consequence, many groups of ferns diversi- fied not only at the level of species but in terms of life habits. The more complex architectures, such as trees with false trunks, lianas, and aquatic ferns, are not diverse and never have been, re- gardless of the clade in which the habit evolved. The evolutionary, and hence ecological, strength of the ferns has been the long persistence of ground cover forms with minimal morphological specialization, providing a pool of ancestors from which more derived growth habits could evolve and specialize ecologically. This potential appears to remain in the group at large and may be the major explanation for their continued diversity. Acknowledgements We thank Mary Parrish for the artwork and Dan Chancy for assistance with preparation of the photographic plates. For constructive comments on the manuscript, we thank Jean Galtier and Barry Thomas. This is Contribution Number 85 from the Evolution of Terrestrial Ecosystems Program at the National Museum of Natural History, which provided partial support. 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