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Review of Palaeobotany and Palynology 119 (2002) 1^33 Ecological strategies in fern

Review of Palaeobotany and Palynology 119 (2002) 1^33

Review of Palaeobotany and Palynology 119 (2002) 1^33 Ecological strategies in fern

Ecological strategies in fern evolution:

a neopteridological overview

Christopher N. Page a;b;

a Royal Botanic Garden, Edinburgh, UK b Cornwall Geological Museum, Penzance TR182QR, UK


Drawing inferences about the past from the ecology of living organisms is one of several approaches to reconstructing palaeo-environments. Pteridophytes are a major component of fossil floras, but their use as environmental indicators is constrained as much by lackof ecological data on living species as by an understanding of

the distribution of fossils. Taking a neobotanical perspective, this paper discusses some important ecological strategies of ferns and allied plants and their underlying selection pressures, based on an extensive survey of tropical and temperate species and on horticultural experience of the behaviour of wild species in experimental cultivation. Broadly parallel developments to similar selection pressures and environmental responses have been sought from amongst distantly related extant families, to derive broad concepts of weaknesses and strengths inherent in the biology of these plants. From this evidence, seven main limitations and twelve important advantages imposed on pteridophytes by aspects of their biology are identified as follows:


b The handicap of an independent gametophyte stage


Single growing-point limitations of sporophyte architecture


Slow plant growth rates


Intolerance of widely fluctuating conditions


Poorly controlled evaporative potential


Uncontrolled high reproductive commitment



Need to ‘return to the water to breed’ b Low-light photosynthetic ability


Diverse phytochemical armament


High disease resistance under saturated humidity levels


High tolerance of acute nutrient disequilibrium substrates


High migrational ability of the airborne spore


Spore tolerance of adverse aerial environments


Flexibility of breeding systems to match varying ecological opportunity


Revivalist tendencies of certain gametophytes


Potential longevity of resultant sporophytes


Exploitation of mycotrophy


Exploitation of potentials of polyploidy


Biotic independence

* Address for correspondence: Cornwall Geological Museum, Penzance TR18 2QR, UK

0034-6667 / 02 / $ ^ see front matter 2002 Elsevier Science B.V. All rights reserved. PII: S 0 0 3 4 - 6 6 6 7 ( 0 1 ) 0 0 1 2 7 - 0


C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33

It is argued that collectively these weaknesses and strengths provide a broad framework, which, operating in varied combinations, limit or open opportunities for exploitation of a considerable array of ecological habitats by Pteridophyta. Based on these data, several general ecological principles are developed. It is proposed that, through time, such strategies are likely to have opened many pteridophyte habitat opportunities, though not all of these will necessarily have left directly identifiable signals in the fossil record. Modern fern ecological limitations and advantages are shown to occur across broad taxonomic spectra and many are innate abilities of the plants. It is, therefore, argued that a similar general frameworkof weaknesses and strengths is likely to have operated in the past, and thus have been of similar relevance in defining and promoting the ecological achievements of the fossil pteridophytes in relation to selection pressures and consequent adaptations. This opens up the potential to extrapolate from the modern ecology for interpretation of palaeo-ecology and palaeo-environments. Examples of this potential are given for each limitation and advantage, where possible incorporating evidence from the fossil record. 2002 Elsevier Science B.V. All rights reserved.

Keywords: Pteridophyta; limitations; strengths; consequent adaptations; ecological and environmental interrelationships; palaeo- botanical implications

1. Introduction

Pteridophyta are a major component of fossil £oras. In interpreting environmental relationships of these plants, we are faced, on the one hand, by a good and very long fossil record through a great diversity of global habitats. On the other hand, there are some 12 000 or more living species of ferns alone (plus horsetails and clubmosses) in a world-wide array of extant habitats. Of the living species, we have good world-wide morphological, taxonomic and phylogenetic information bases, but we are only just beginning to askquestions about the more subtle aspects of their ecologies and the reasons behind the adaptations and the architectures that we see. In comparing the living and the fossil, it is im- mediately clear that there is much common ground. However, it is also clear that not every palaeo-problem is necessarily answered by the liv- ing plants, in the same way that not every prob- lem of origin of the living plants is necessarily answered by the fossil record. Both ¢elds have their unique strengths, and provide complementa- ry approaches, between which information bridges can help to add important additional in- terpretative elements. To assemble even the baseline account of extant fern ecology presented here, it is ¢rst necessary to construct a skeleton of ideas and proposals which can be tested against evidence. It is then necessary to draw together information from a highly scat-

tered world-wide literature, both pure and ap- plied. There are a wide variety of relevant data (e.g. from biochemical to biotic, from edaphic to climatic, and from physiological to genetic and mycological) which need careful evaluation and sensitive interpretation. These data must be re- lated to direct observations of both whole fern communities and individual species niches in the ¢eld (especially in the wet tropics). Autecological information is added from life-cycle observation in experimental cultivation. A synthesis of resul- tant data is necessary against the taxonomic spec- trum to which it might apply today, with constant awareness of the areas likely to be of particular palaeo-relevance. It is also vital to be aware of what is not known or has been inadequately studied which, even in living ferns, is manifold. This account focuses particularly on ferns, although relevant comparable data from other pteridophyte groups (horsetails and clubmosses) are added where appropriate and available. The account draws on nearly 40 yr of personal ¢eld ecological observations and experimental study of ferns. Identi¢ed and itemised on the basis on this evidence are: (1) the intrinsic limitations to fern ecological success (Section 2: Intrinsic limitations to fern ecological success); and (2) the important advantages imposed on pteridophytes by aspects of their biology, which establish recurring strat- egies of fern ecology, adaptation and survival (Section 3: The recurring advantaging strategies of fern ecology, adaptation and survival). These

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/ Review of Palaeobotany and Palynology 119 (2002) 1^33 3 Plate I. A monospeci¢c stand of

Plate I. A monospeci¢c stand of Pteridium aquilinum (bracken), demonstrating the ability of colony-forming forest margin ferns to respond, aggressively and extensively, to environmental factors which open habitats. In this case, the response is to human im- pact (severe over-grazing by livestockminimising natural tree regeneration).

enable ferns, despite the limitations, to occupy and succeed in a wide range of ecological niches today. An example of this success is the forest margin colony-forming fern like Pteridium (brack- en) in Plate I. Both the limitations and the strategies are di- verse. In de¢ning these, broadly parallel examples of ¢eld situations and responses have been docu- mented from among members of unrelated fern families (both Leptosporangiate and Eusporan- giate) in multiple locations in response to similar selection pressures. This provides a resource-rich information base, which points to principles of modern fern ecological survival abilities which have potential to translate into broader palaeo- settings. It is not suggested that all interactions between fossil ferns and their palaeo-environments have necessarily always been identical to those of to- day, since selection pressures, especially of a bi-

otic origin, have varied. Furthermore, it is ac- cepted that not all habitat possibilities under which fossil taxa have existed necessarily still ex- ist. Many taxa are also now extinct (DiMichele and Phillips, 2002). Nevertheless, it is proposed that similar overall strategies are likely to have operated as regular features of palaeo-fern adap- tation, in response to generally similar past selec- tion pressures whenever palaeo-events and palaeo- opportunities and constraints have promoted these.

2. Intrinsic limitations to fern ecological success

A variety of intrinsic limitations to fern ecolog- ical success handicap ferns today, and have prob- ably always done so. Appreciation of these limi- tations is essential to an understanding of the strengths of the ecological strategies, which have


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then been achieved despite them. Seven such fac- tors are de¢ned here. Virtually all of these apply broadly to all fern groups although, inevitably, a few (but usually only a few) species have adapted to circumvent the disadvantage of at least some of these handicaps. This was probably also true in the past.

2.1. The handicap of an independent gametophyte stage

Restrictions imposed on the sporophyte by the occurrence, in the life cycle, of an independent gametophyte stage are at least twofold:

(1) Collectively, the successful arrival, germina- tion, and establishment stage provides an ‘achilles heel’ to the whole fern life cycle, and is probably the stage at which the greatest numbers of indi- viduals (by an order of magnitude) fail and be- come eliminated on a regularly recurring basis in the ¢eld. (2) Among the few successful establishees, the resulting gametophyte determines the general site of origin of the sporophyte, whether this be opti- mal or not for the subsequent vascular genera- tion. High and fortuitous roles of chance and sharp levels of selection pressures would seem to pro- foundly characterise these normally short-lived stages of the fern life cycle, while the process of fertilisation itself is also dependent of the addi- tional presence of adequate free-water (see Section 2.7: Need to ‘return to the water to breed’). Be- tween such very di¡erent organisms as the non- vascular prothallus and free-living vascular spo- rophyte, it would seem likely that evolutionary

pressures would tend to worktowards achieve- ment of some degree mutualistic equation of hab- itat tolerance. A few extreme cases are known which serve to show a little of the range of com- plexities which may become involved. These in- clude the occurrence of apogamy, which produces sporophytes without fertilisation (Walker, 1979), delayed sex expression (Duran and de la Sota, 1996), occurrence of clonal gemmiferous gameto- phytes (Dassler and Farrer, 1996), and occurrence of pH metamorphosis between gametophyte and subsequent developing sporophyte in Pteridium (Page, 1986). In ferns with independent gameto- phyte stages, marked contrast exists between the ecologies of the gametophyte and sporophyte (Farrar, 1967, 1985; Pecket al., 1990; Rumsey et al., 1992; Rumsey and She⁄eld, 1996). Consequences may include enabling species to survive under conditions which are at times un- suitable for sporophyte formation or sporophyte survival (see also Section 3.11: Exploitation of potentials of polyploidy). Such potentials, which can be far from ‘textbook’, need to be borne in mind in the interpretation of the breadth of pte- ridophyte adaptation, especially to more unusual palaeo-habitats.

2.2. Single growing-point limitations of sporophyte architecture

In great contrast to the multi-growing points of many angiosperms, the single growing-point of the pteridophyte rhizome (whether it is a terres- trial or aerial ‘stem’) becomes the whole basis for the origin and direct tenure of not only roots but also all leafy and fertile parts of ferns. Consider-

Plate II. Examples of ecological advantages in ferns. (1) The retention of a ‘skirt’ of persistent fronds in Dicksonia antarctica lim- its the upward progress of potential climbers and epiphytes, preventing them from damaging the single growing point of the mo- nopodial tree fern crown. (2) Perfect undamaged fronds and unusual odours occurring in the genus Anemia re£ect the complex phytochemical armament in ferns. (3) Woodwardia radicans thrives on steep ravine sides of dense laurel-forest interiors in the Canary Islands and is one of many forest interior ferns showing tolerance of low levels of illumination. (4) The delicate membra- neous fronds of the fern Hymenophyllum are typical of the family Hymenophyllaceae, which grow under saturated humidity levels (e.g. cloud zones of tropical mountains), show little decay or damage indicating their high disease resistance even under these conditions. (5) Some taxonomically outlying ferns, in families with a long fossil history and unusual and characteristic morphol- ogy, are virtually exclusive today to extremely poor edaphic substrates. This Dipteris conjugata, for example, thrives forming groves on the leached gleyed-clay soils of tropical high mountain ridges and saddles in south-east Asia. (6) Asplenium septentrio- nale, is one of many ferns tolerant of rocks with potentially toxic levels of minerals, especially metals.

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able vulnerability is consequent should that grow- ing point become damaged, and this basic archi- tecture can also limit the £exibility of morpholog- ical response (Gureyeva 2001). Additionally, damage response, through development of new lateral growing points as side-rhizome out- growths, is usually slow. Main avoidance mecha- nisms, which at least partly circumvent this innate vulnerability, include:

(1) physical structure: this includes density of hairs, scales and occasional spines to protect the young expanding croziers; (2) removal of growing points to high above the ground, such as in tree ferns: this avoids tram- pling and direct foraging interest especially by small- to medium-sized tetrapods; (3) branching of the rhizomes: this provides multiple rhizome-apex survival opportunities; (4) concentration of great species diversity in sites of low browsing (and trampling) encounter:

¢de the great success of lithophytes and epiphytes among ferns; (5) high emphasis on biochemical armament ap- parently e¡ective against a broad-spectrum of an- imal taxa: see Section 3.2: Diverse phytochemical armament. In the case of tree ferns, particular vulnerability then ensues from the creation of a trunkwhich is itself a desirable habitat for colonisation by other plants, notably by climbing epiphytes and scram- bling lianes. All of these are harmful to tree ferns since the inevitable upward growth of each is drawn directly towards the single monopodial tree fern crown. Further architectural develop- ments by the tree fern are needed to counter these advances. Two methods are adopted widely by existing tree ferns. Some produce fast upward growth resulting in a slender trunkwhich itself has a smooth polished surface (with clean frond abscission leaving only smooth leaf scars) upon which it is di⁄cult for climbers to gain purchase. Others, such as Dicksonia (Plate II, 1) and some members of the Cyatheaceae and Blechnaceae, have slow upward growth (resulting in a thicker and more rough-surfaced root-clad trunk), but they retain dense ‘skirts’ of old fronds hanging below the crowns. These act as a foil to ascending climbers and epiphytes which substantially fail to

negotiate round or through this ‘skirt’ (Page and Brownsey, 1986). Such crown vulnerability will have been char- acteristic of ferns through the whole of the fossil record, through which similar (and perhaps other) strategic avoidance mechanisms will have been elaborated. The presence of either exceptionally clean trunks to fossil tree ferns or the presence of persistent tree fern skirts would itself indicate defensive mechanisms against the presence of climbers or epiphytes in the associated palaeo- £ora. It would seem that the Palaeozoic tree fern Psaronius used neither of these deterrents ef- fectively as it was colonised by both epiphytes and climbers (Ro« ssler, 2000; DiMichele and Phillips, 2002-this issue) though these may have been re- stricted to the lower part of the trunk.

2.3. Slow plant growth rates

Sporophyte (and sometimes gametophyte) growth rates can vary widely between di¡erent fern groups, speci¢c taxa, parents and allopoly- ploid o¡spring (see Section 3.11: Exploitation of potentials of polyploidy). They can also vary in relation to location and habitat positioning within the same species (e.g. Cousens, 1981). Neverthe- less, in comparison with many angiosperms, over- all fern growth rates are relatively slow (least so in some epiphytes and some pioneer species), and this has been suggested to be linked to the inher- ently slow rates of some physiological processes in ferns (Raven, 1977, 1984, 1985a). These include, water movement in the xylem of purely tracheid- based construction (Woodhouse and Nobel, 1982; Gibson et al., 1985); di¡usive resistance (Wong and Hew, 1976) and conductance of photosyn- thetic carbon assimilation in mainly C3 pterido- phytes, which are considered ‘‘generally towards the low end of the range’’ for terrestrial tracheo- phytes (Raven, 1985b). Constraints imposed by growth rates in associ- ation with the pteridophyte life-cycle (see Section 2.1: The handicap of an independent gameto- phyte stage) also limit the capacity of pterido- phytes to adopt short life-cycle turnovers of the type which have enabled mosses as well as £ower- ing plants to evolve small ephemeral forms (Ra-

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ven, 1985b; Richardson, 1992, p. 98). This is sup- ported in conditions of experimental cultivation where only a few exceptional examples have been met which display rapid life-cycle turnovers of the order of a year or less from spore-sowing to sporophyte ¢rst spore production. These occur in a few ‘modern’ genera (such as Anogramma and Pityrogramma (both Gymnogrammaceae) and Doodia (Blechnaceae)) and represent under 0.2% of taxa personally cultivated in 40 years. Annuals are thus rare in pteridophytes as a whole, and the very great majority of ferns are thus committed perennials, with inherently longer life-cycle turn- overs (and often years to maturity) that this im- plies. Such multi-year perenniality seems likely to have also been the case for most ferns in the past. Furthermore, there is also a general trend for greatest longevity to be achieved amongst sev- eral taxonomically more ancient extant taxa (e.g. Osmunda, Angiopteris, Equisetum), which may mean that longevity may have been an even great- er feature of even more pteridophytes in the fossil record. That this is usually coupled to ultimate size achieved should allow for appropriate fossil signals to be identi¢ed and perhaps community age-structure to be indicated, and might further indicate palaeo-sites of adequate habitat stability (see also Section 2.4: Intolerance of widely £uc- tuating conditions). Occurrence of multi-aged populations, including aged individuals, would imply continuing habitat stability, and where re- inforced by representation within the same com- munity of high taxonomic and morphological di- versity, would clearly indicate climax palaeo- communities with multiple niche opportunities. This seems to have been the case for some Palaeo- zoic marattialean communities (DiMichele and Phillips, 2002-this issue).

2.4. Intolerance of widely £uctuating conditions

Intolerance by unadapted sporophytes of widely £uctuating conditions is a particularly under-appreciated ecological limitation of the ma- jority of ferns (Watt, 1976; Arens and Baracaldo, 2000). Fronds of most extant ferns (perhaps all), appear to be able to make a once-only commit-

ment, such as on emerging, to habituation to am- bient environmental conditions: light regimes, moisture levels, air movement rates (Page, person- al observations). Expanding fronds adapt to these at the levels at which these environmental in£uen- ces are met on initial frond expansion. Should conditions subsequently change (such as increase in light levels due to a tree fall gap forming in the canopy) existing fronds appear unable to re- adapt. Only subsequently emerging fronds adapt as far as they are functionally able to the new conditions encountered. Plants may require a full growing season before all fronds borne be- come modi¢ed to any major features of environ- mental change. Furthermore, lackof stomatal control, should conditions change, has been docu- mented in Lycopodium species, with modest amounts of inter-speci¢c variation (Heiser et al.,


Established sporophytes thus do not respond well to environmental £uctuations, unless they are ones to which a species is especially pre- adapted. It is probably such inherent incapabil- ities of short-term response that ensures that fern sporophyte success is always greatest when environmental conditions (of virtually all types) remain most constant. As a widely encountered example, it is almost certainly for these reasons that, in temperate cli- mates, fronds are delayed in emergence until the tree canopy itself has mostly completed growth (Page, 1988). Little would be achieved, and there is everything to loose, by timing frond-expansion to be any earlier than this. In tropical moist cli- mates, however, where there is year-round forest canopy shade-provision, new fern frond growth can occur throughout the year. By contrast to the single spring growth ‘£ush’ of fern frond emergence of temperate regions, tropical fern fronds arise typically in a steady and sequenced year-round succession, accommodating ample op- portunity for subsequent adaptation to any envi- ronmental changes which do arise. Other varia- tions occur in tropical dry climates, and in all sites, further micro-habitat variations appear to be involved. An interesting tropical example, The- lypteris angustifolia, is being very closely docu- mented by Sharpe (1996), in which seasonal rain-


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fall patterns are closely re£ected in subsequent development patterns of the plant. Such patterns may well have considerable bioindicator value, and need more detailed study. If this fern preference for constant environment also prevailed in the past, as seems likely, then palaeo-environmental conditions can be inferred from fossil fern £oras. For example, fern crowns with fronds and frond buds simultaneously at

In Equisetum, Equisetum £uviatile tolerates the most anaerobic (and still) water conditions, while at the other extreme, Equisetum telmateia requires the most oxygenated water, and is indicative of constantly moving water sites (such as especially that below springlines Page, 1988, 1997b). Such aspects of micro-habitat di¡erences must also ap- ply to many pteridophytes in other sites. Climatic factors especially closely in£uence

2.6. Uncontrolled high reproductive commitment

multiple stages of development (either on individ- ual specimens or within populations) would be usefully indicative of stability within a growing- season (and could lead to an estimate of growth- season length, such as in the wet tropics today). By contrast, frond buds simultaneously at the same stage would indicate growing-season release within a more seasonally £uctuating environment.

pteridophyte success and di¡erentiate closely be- tween that of di¡erent fern species. These include, in particular, such factors as frequency of precip- itation and its temporal distribution (i.e. not just overall amount), degree of exposure versus shel- ter, and factors linked more indirectly to evapo- ration such as cloud-cover. There is, as yet, re- markably little accessible data on most of these


further signal reinforcing the latter, but in the

aspects even for living pteridophytes. It requires

non-growing season, might be the additional pres- ence of seasonally developed subterranean storage organs. Root tubers on some ferns (e.g. Adian- tum), if fossilised, would indicate dislodgement during a dry-season interval. Equisetum, where clearly fossilised with tubers, would indicate fos- silisation in winter (between September and early April in the northern hemisphere), and that the aerial parts would have been deciduous and thus not simultaneously present.

diligent e¡orts to draw such information together even for well documented areas such as Britain and Ireland (see, for example, maps of several factors especially signi¢cant to pteridophytes gen- erated on long-term accumulated data by the Brit- ish Meteorological O⁄ce in Page, 1982b). There is considerable potential to exploit pter- idophytes as discriminating and sensitive environ- mental indicators, both for the present and the past, using approaches being more widely devel-

2.5. Poorly controlled evaporative potential

oped (and funded!) mainly by agro-meteorologi- cal and forestry sources (see especially Thompson

The general need for moist environments, with low evaporative potentials to counter high rates

et al., 2000). Fern £oras and nearest living rela- tives (‘indicator species’) could both be applied in palaeo-environmental studies. Environmental in-


water loss, characterises much of the life-cycle

dicators could be used, for example, for establish-


the majority of ferns (e.g. Wylie, 1948). This

ing relative comparisons between habitats and

problem places often severe limitations on the de- gree of exposure which can be tolerated by many ferns. Such poor control clearly restricts pterido- phyte and especially fern success on both a re-

niches in separated palaeo-locations (cf. the mod- ern Equisetum example cited above).

gional and a habitat basis, and is certainly also highly taxon-speci¢c. It is a noteworthy aspect of this limitation in living fern taxa, that individual species are often limited by particular levels of soil-water availability, as well as surrounding air humidity. Furthermore, even within the same habitat, di¡erent species can have subtly di¡ering requirements, including lateral movement and particular aeration levels of the soil water present.

Nearly all pteridophyte sporophytes, including ferns of most genera, have a high and largely un- controlled annual reproductive commitment. Once an appropriate stage of maturity for an in- dividual sporophyte has been reached, spores are typically produced in prodigious numbers throughout the remaining life of the plant. This may be over decades or more (Gureyeva 2001).

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As a consequence of this production rate, extra- ordinary levels of over-saturation must regularly occur in terms of what is necessary to maintain individual populations within existing commun- ities, where the great majority of spores must in- evitably fall (e.g. Conant, 1978; Dyer and Lind- say, 1992; Bernabe et al., 1999). The price of such over production, and the inability of most ferns to control it, must be a considerable drain on recur- rent energy commitments by the parent sporo- phyte. These levels of commitment, the apparently highly sacri¢cial nature of much of the process, and the fortuitous roles of chance are probably little di¡erent in character today from those which typi¢ed the life histories of ferns through their long palaeo-history. This disadvantage is, however, a two-edged sword, since some clear advantages may well also be gained by large spore numbers. These are dis- cussed in Section 3.5: High migrational ability of the airborne spore. Of these, signi¢cant in a pa- laeo-perspective are likely to be combinations of recurrent arrival at sites of poor access, abilities of potentially long-distance dispersal, and of rapid exploitation of sites immediately following post- disaster scenarios. All, and especially the latter, open opportunities for serial successions to begin to involve pteridophyte sporophytes from the ear- liest stages, in potentially large numbers. These have, through the fossil record, doubtless greatly in£uenced the overall ability of pteridophytes (and especially ferns) to become exploiters of the epiphytic niche. However, this may seldom be a habitat of high preservation potential (Poole and Page, 2000) and is hard to document in the past (DiMichele and Phillips, 2002-this issue).

2.7. Need to ‘return to the water to breed’

The need for the existence of free water, even if only as a ¢lm, is essential for sexual fertilisation by free-swimming motile antherozoids within the immediate habitat niche in which the prothalli of the gametophyte generation actually grow. Apart from in the example of occasional apomictic ga- metophytes (see Section 3.7: Flexibility of breed- ing systems to match varying ecological opportu- nity), reproduction for most pteridophyte species

is thus limited to occasions and locations when such free water exists. Observations in experimen- tal culture (Page and Walker, independent person- al observations) show that for some species this may be as ¢nely tuned as speci¢cally timed an- therozoid release (and perhaps archegonial recep- tivity) over only certain periods in seasonal and even diurnal cycles, with which such free water has to necessarily coincide. This is a little-appre- ciated factor which may well contribute substan- tially to detailed delimitation of pteridophyte niches, habitats and overall ranges, as well as hy- brid occurrence (and thereby evolutionary success (see Section 3.11: Exploitation of potentials of polyploidy). In this respect, the Pteridophyta as a whole are very much the plant Kingdom’s equivalent of the Amphibia, between which there are many broad similarities in ecology, life-style, tropical diversity, habitat range, moisture limitations and the con- tinuing occurrence of a free-living ‘juvenile’ phase (Page, 1985). Such similarities and limitations must have applied at least equally strongly throughout the pteridophyte fossil record, where other pteridophyte^amphibian analogues might also exist. Clearly, for almost all pteridophytes, the achilles heel of a free-water requirement will have been experienced throughout their past history, to the degree that fossil pteridophyte presence is neces- sarily indicative of the presence usually moist en- vironments, in which adequate free-water (chie£y by precipitation) will at some time have been present. To a large extent, pteridophyte taxonom- ic and morphological diversity today is a measure of the regularity and reliability of occurrence of such water ^ ¢de the overwhelming abundance which ferns can achieve in the regularly moist cloud zones of tropical mountain mist forests to- day. (This limitation clearly links closely to that of Section 2.4: Intolerance of widely £uctuating conditions, and Section 2.5: Poorly controlled evaporative potential, and also to Section 3.3:

High disease resistance under saturated humidity levels). Sites of exceptional fern diversity within the fossil record, coupled with analysis of the eda- phic niches occupied by the species and life-forms involved, can potentially provide a valuable tool


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towards determining aspects of water availability in various palaeo-environments.

3. The recurring advantaging strategies of fern ecology, adaptation and survival

In contrast to the seven limitations above, the advantaging strategies of fern ecology (12 are identi¢ed here as 3.1^3.12) are the ‘positive’ side of fern potentials, adaptation and survival. These compliment those of the ecological approach of Grime (1977, 1985). These strategies re£ect recur- ring pteridophyte strengths today and are likely to have done the same throughout the history of pteridophytes. In deriving an analysis of these strategies, the extant ferns provide a resource-rich information base, in which laboratory workand experimental cultivation each contribute a substantial experi- mental database. The evidence is combined here with information from the ¢eld to achieve an overall broad ecological synthesis. The evidence supports the view that many clear and de¢nable principles of survival exist amongst extant fern taxa, governed by innate abilities of the plants themselves, and which occur across broad taxo- nomic spectra.

3.1. Low-light photosynthetic ability

Virtually all observational fern ecology today would support the view that many ferns survive particularly well in levels of light which are too low for most competing angiosperms (as well as many conifers) to tolerate, but I am aware of few exacting physiological measurements which ad- equately quantify this. Complete photosynthetic saturation at low levels of incident light would appear to be the key factor (Page, 1979b). Arina- wati et al. (1996), for example, quote high total chlorophyll levels and particularly low light-satu- ration photosynthetic rates of fronds of the trop- ical climber Teratophyllum rotundifoliatum (which has fronds in both low and high light levels), and indicate that di¡ering in£uences of light type may also be involved. Fern species of low-light habitats (which are

very many, e.g. Plate II, 3) exploit a niche in which competition pressure today is substantially reduced. These abilities undoubtedly greatly facil- itate the occupation of a wide range of niches in forests, from deep shaded ravines to darkforest £oors, as trunkepiphytes and climbers, and as plants of highly cloudy or frequently misty envi- ronments. Low light-saturation e⁄ciencies will have been a particularly important factor through the course of angiosperm radiation (e.g. Crane, 1987). Such shade-tolerating potentials have al- most certainly been available to ferns in habitats of earlier forest types too (e.g. Thomas, 1985) and could well have evolved, for example, as adapta- tions to highly cloudy and misty environments, very long before angiosperm diversi¢cation. Probable forest-£oor shade tolerant taxa (on the basis of their nearest living relatives) are known in some palaeo-£oras (e.g. Rothwell et al., 1994; Stockey et al., 1999). Large and delicate fern fronds are also represented in the fossil rec- ord (e.g. Deng, 2002-this issue) and so are ferns of the shaded woody habitats of peat-forming swamps (Collinson, 2002-this issue; DiMichele and Phillips, 2002-this issue; Van Konijnenberg- van Cittert, 2002-this issue). However, ferns of shade habitats are, from evidence of living species, frequently soft and/or thin-fronded and of gener- ally delicate texture. Plants of such structure (es- pecially extremes like Hymenophyllaceae) would seem to o¡er a particularly low potential to nor- mally become well-represented (at least as macro- fossils) in most fossil £oras. By contrast, the coarser-textured often higher biomass, tough structures (especially stipes) and frequently more monospeci¢c counterparts (e.g. Plate I) of more open habitats have higher fossilisation potential (e.g. Collinson and Ribbins, 1977; Yao and Tay- lor, 1988; Skog, 1992; Rees, 1993; Gandolfo et al., 1995; Cantrill, 1996). (Today, these ferns in- clude genera such as Dennstaedtia, Lonchitis, His- tiopteris, Hypolepis, Paesia, Pteridium.) This ta- phonomic bias should be taken into account when interpreting fern £oras of the past.

3.2. Diverse phytochemical armament

Mostly only becoming known in the last 25 yr,

C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33


diverse phytochemical armament is probably the most e¡ective and widespread strategy in promot- ing direct vegetative survival of Pteridophyta as a whole. It is becoming clear that phytochemical armament, of widely di¡ering degrees and types, is taxonomically widespread in ferns and other pteridophytes, and appears to be the prime anti- herbivore grazing defence mechanism of both gen- erations. Such biochemical armament has clearly become an e¡ective route of defence for such a predom- inantly herbaceous group with relatively slow growth rates (see Section 2.3: Slow plant growth rates), vulnerable growing points and organs and lackof most other physical defences or herbivore avoidance mechanisms (see Section 2.2: Single growing-point limitations of sporophyte architec- ture). It probably also contributes substantially to the survival of gametophytes, and thus to mitigat- ing against the apparent vulnerability of this free- living stage (see Section 2.1: The handicap of an independent gametophyte stage). Such biochemi- cal armament, however, undoubtedly requires continuing resource and energy commitments on the part of the plant, but it avoids the need for development of elaborate physical defence struc- tures, thus enabling relatively simple pteridophyte architectural form to persist. Nevertheless, remarkably little is yet under- stood about which of any known phytochemical substances are employed to achieve e¡ective de- fence and exactly what they are targeted against. Currently we are only aware that present targets seem broad, and were probably similarly so in the past. Field botanists will be aware, however, that few modern ferns usually show signs of any sig- ni¢cant herbivory in the ¢eld. Even to a human nose, many ferns have distinctive (and often spe- cies-speci¢c) odours (e.g. Plate II, 2), some of which are quite curious: e.g. the temperate Gym- nocarpium robertianum (Athyriaceae) which has an apple-like fragrance, Polypodium glycyrrhiza (Polypodiaceae) which smells of liquorice, and the tropical Anemia phyllitidis (Schizaeceae) which smells to me of running model railways!). The research which is available suggests that, in most ferns, general browser interest appears to be suc- cessfully checked (or at least, held to a minimum)

by cocktails of biochemical repellent pathways in- volving sometimes complex chemical components (Bohm and Tryon, 1967; Hayashi et al., 1977; Cooper-Driver, 1978, 1985; Balicket al., 1978; Jones and Firn, 1978, 1979; Gerson, 1979; Had- ¢eld and Dyer, 1986; Suksamrarn et al., 1986; Smith et al., 1990). Sporophytes of Bracken (Pteridium) have been more extensively studied in this respect than any other fern, and provide a valuable generic exam- ple. Pteridium is known to contain a particularly formidable armoury of repellents, from tannins and sesquiterpenoids to phenols and cyanide (as a cyanogenic glycoside), plus two carcinogens, a leukaemiagen and, for good measure, a broad- spectrum insect ecdysone. Collectively, or sepa- rately, these can have dire e¡ects on potentially browsing animals of many types (e.g. Harding, 1972; Cooper-Driver and Swain, 1976; Evans, 1976, 1986; Hendrix, 1977; Temple, 1981; Schreiner et al., 1984; Fenwick, 1988; Had¢eld and Dyer, 1988; Saito et al., 1989; Galpin et al., 1990; Low and Thomson, 1990; Smith et al., 1990; Wells and McNally, 1995; Bronstein, 1998; Thomson, 2000). Allelopathic compounds, toxic to other plant growth, are also copiously produced by bracken (e.g. Gliessman, 1976; Gliessman and Muller, 1972) and probably by many (? most) ferns (Weinberg and Voeller, 1969; Banerjee and Sen, 1980). Furthermore, at least in Pteridium, the spores also are known to be substantially armed with some of the same com- pounds in even higher concentration per dry weight than in the vegetative body of the plant (Evans and Galpin, 1990). These compounds are presumably e¡ective against sporophagy during both pre-dispersal and post-dispersal phases. Fern fronds can and do, however, provide roosting-habitats for a great number of terrestrial arthropods (e.g. Lawton, 1976; Gerson, 1979; Ot- toson and Anderson, 1983; Lawton and MacGar- vin, 1985; Brown, 1995; Jensen and Holman, 2000) with which the plants appear to successfully co-exist. A limited tolerance to a degree of grazing appears to exist between ferns and some insects, notably Lepidoptera and sometimes Hemiptera (Balicket al., 1978; Lawton, 1982; Lawton and MacGarvin, 1985; Weintraub et al., 1995). Addi-


C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33

tionally, various ant^fern associations and mutu- alisms are becoming recognised (e.g. Darwin, 1877; Southwood, 1977; Page, 1982a; Lawton and Heads, 1984; A.F. Tryon, 1985; Walker, 1985; Arens and Smith, 1998). Sometimes further defensive bene¢ts to the plant may be gained by tolerating the presence of such animals, and some defence mechanisms, expensive in energy invest- ment, may be discontinued when not needed. An example of this is in the specialist myrmeco- philous epiphytic Lecanopteris carnosa (Polypo- diaceae). Experience in glasshouse cultivation (Page and Walker, personal observations, 1964^ 1967) shows that this species has prothalli and young sporophytes which are especially attractive to rapid and usually terminal depredation by small slugs. However, in the wild, this species is regularly and aggressively ant-colonised (and is here inferred to be likely to be mutualistically ant-protected) on the branches of the tropical lowland swamp-margin trees on which these large epiphytes normally grow (Jermy and Walker, 1975). It is presumed here that chemical defences have been dropped when other alternative (less energy-consuming) defence mechanisms have be- come available. Our observations showed that the same slugs and snails did not similarly attacka broad range of other adjacent fern cultures. This provides at least some negative evidence of a nor- mal defence in most pteridphytes (presumably chemically mediated) which would appear to be sensed, and thus avoided, by slugs, snails and pre- sumably other invertebrates. Some of the e¡ects of pteridophyte chemical constituents today are responses to potential mi- crobial attack(e.g. Kobayashi et al., 1975; Baner- jee and Sen, 1980). However, it is mainly against browsing pressures, especially by arthropods (e.g. Wootton, 1981, 1990; Scott et al., 1985, 1992, 1996) that selection pressures for the development of such a diverse array of phytochemical arma- ment (and a diversity of arthropod counter-mea- sures) will have been recurrently stimulated. Very few other ferns have been studied in any compa- rable detail to Pteridium, although the list of taxa and known phytochemical isolates and their di- versity of e¡ects on modern browsing animal groups is steadily growing. The extent of these

indicates a high probability that such defences are general in most living pteridophytes. They can be varied (e.g. through a number of di¡erent secondary compounds focussing especially, though not exclusively, on a diverse range of cy- clopropane compounds ^ Potter, 2000) and pro- mote, amongst other e¡ects, onset of degenerative conditions in a broad spectrum of animals expe- riencing them. Other contained compounds, such as ecdysones, are more arthropod-speci¢c. Also essentially phytochemical in origin (and almost worthy of a separate entry as a further independent advantaging attribute of ferns, were there clearer evidence), is the occurrence in ferns of chemically unusual intra-cellular cements, which bind cells together (Manton, 1950). As far as I am aware, in contrast to all phytochemically toxic aspects of ferns, nothing is known about these, beyond that they contrast with those of all £owering plants. In ferns, these have the repute of not being soluble in hydrochloric acid, and of hence making fern frond material indigestible to all animals dependent on an HCl-mediated diges- tive system. Indeed, slugs and snails are the only animals known (at least by repute amongst pter- idologists) to have the necessary stomach enzymes with which to attackthese fern cements. I person- ally regard this as a potentially important survival strategy in ferns (and possibly in other pterido- phytes) against animal depredation, but, so far as I am aware, the whole topic appears virtually unresearched. It could, however, have consider- able implications both for the survival of ferns against a range of herbivores through time. Fur- thermore (especially if it also operated against de- cay organisms ^ I do not have any evidence either way), it may also have a¡ected the preservation potential of ferns throughout the fossil record. Pteridophytes as a whole have been the focus of general browsing attention (including detritivory) especially from invertebrates (such as Oribatid mites ^ Labandeira et al., 1997) since the Carbon- iferous or earlier (e.g. Scott and Taylor, 1983; Jeram et al., 1990; Stephenson and Scott, 1992; Scott et al., 1985, 1992, 1996; Jarzembowski, 1994; Collinson, 1996; Labandeira and Phillips, 1996; Labandeira, 1998). There are some indica- tions, from Palaeozoic compression £oras, that

C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33


fern leaves were already then less browsed than alternative vegetation (e.g. Beckand Labandeira, 1998; Collinson, 1996, p. 380^381) and, although the Palaeozoic tree fern Psaronius exhibits a host of arthropod interactions these do not seem to include leaf-feeding (Labandeira, 2001). During this long period of interaction, evolutionary pres- sures for the development of adequate armament must have been intense, constant and diverse in most habitats in which Pteridophyta have suc- ceeded. Clearly modern ferns enjoy considerable abilities to achieve complex biochemical defence potentials (e.g. Hartzell, 1947; Evans and Mason, 1965; Hayashi et al., 1977; Swain and Cooper- Driver, 1981; Ojika et al., 1987; Saito et al., 1989; Kushida et al., 1994; Castillo et al., 1997; Potter, 2000; Siman et al., 1995, 2000). Doubtless many other variations have occurred through the fossil record against the same selection pressures. Increasingly, evidence is that the pathways of known defence involved are, chemically speaking, complex; biologically speaking, e¡ective; and evolutionarily speaking, diverse and often subtle. The main measure of the speci¢c e⁄cacy of bio- chemical defences through the fossil record is most likely to be gained through assessments of actual recordable incidences (and hence inferred susceptibility) of browsing activity (foliar/spore) between contemporaneous taxa and through time (like that of Wilf and Labandeira (1999) for angiosperms). Unfortunately, for the fossil record, those taxa which were highly susceptible will be those least likely to be represented. How- ever, clearly the Pteridophyta are not mere begin- ners at these diverse and extensively practised achievements!

3.3. High disease resistance under saturated humidity levels

Once past the life-cycle hurdles of spore surviv- al (including possible survival as soil spore-banks ^ see Dyer and Lindsay, 1992), potential sporoph- agy (e.g. Leschen and Lawrence, 1991) and achievement of successful germination and estab- lishment (see Weinberg and Voeller, 1969; Dyer, 1979; Lloyd and Klekowski, 1970; She⁄eld, 1996 for reviews), ferns succeed under humidity re-

gimes within which most £owering plant seedlings would readily ‘damp-o¡’ through rapid fungal at- tack. Cultivation experience shows that intrinsic pathogen resistance abilities are taxonomically es- pecially widespread in ferns and are expressed ef- fectively in both the gametophyte and the sporo- phyte stage to the great competitive ecological advantage of the fern. Extreme examples must be the ¢lmy ferns (Hymenophyllaceae), many of whose members grow permanently and success- fully in habitats such as the spray-zones of trop- ical waterfalls, where the £imsiness of the fronds (Plate II, 4) might appear to scarcely make a side- salad for a self-respecting pathogen! The mecha- nisms of such tolerance are very little understood, though antibiotic e¡ects have been reported in ferns (e.g. Kobayashi et al., 1975; Banerjee and Sen, 1980). Thin-fronded ‘¢lmy ferns’ (which have been as- signed to the Hymenophyllaceae) are known from the Mesozoic (Deng, 1997; Axsmith et al., 2000) implying a long history for ferns growing in satu- rated humidity levels. Signi¢cantly, many of the ferns in a diversity of distantly related families in this habitat today are successfully bulbiferous, often developing a ‘walking-fern’ habit and/or de- velop axillary branching patterns of growth. Such habits occur in few other habitats, and hence would provide an important marker in the fossil record for such humidity and moisture regimes.

3.4. High tolerance of acute nutrient disequilibrium substrates

Two suites of factors here (which could almost rankas separate advantaging strategies in their own right) operate either independently or collec- tively in achieving unusually high and varied nu- trient disequilibrium tolerance amongst modern ferns. These suites are: (1) a direct ability to tolerate a range of exceptionally low nutrient terrains (e.g. Plate II, 5); (2) an additional ability to tolerate additional unusual levels of excess mineral ele- ments which can also be present in some of these terrains, and which can be at levels that would be toxic to many other plants (e.g. Plate II, 6). Field ecology suggests that these tolerances ap-


C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33

pear to be possessed, either separately or collec- tively, within an especially wide taxonomic array of genera and families of extant ferns (e.g. Con- way and Stephens, 1957; Kruckeberg, 1964, 1976, 1964, 1976, 1984; Holbrook-Walker and Lloyd, 1973; Lloyd, 1976; Kornas, 1978, 1985; Page, 1979b, 1988, 1999; Sleep, 1985; Spicer et al., 1985; Malaisse et al., 1994; Tsuyuzaki, 1997). Within each suite, wide and diverse spectra of actual tolerance levels and types doubtless exist. In the second suite, wide variations in the individ- ual minerals which can be tolerated almost cer- tainly exist, although beyond ¢eld observations, there is yet little available quanti¢ed data on this. Amongst the ¢rst suite, subtle di¡erences amongst tolerances of epiphytic taxa are re£ected in the tendency (in the tropics especially) for dif- ferent pteridophyte epiphytes either to be general- ist or more narrowly specialist species as far as preferred host-tree habitat selection is concerned (cf. Gardette, 1996). Signi¢cantly, in both suites, species with di¡erent apparent substrate preferen- ces (presumed a re£ection of di¡erent tolerances) frequently occur within the same genus. This sug- gests that the detailed tolerances have evolved very numerous times in ferns, adapting individual taxa closely and subtlety to e¡ective exploitation of particular local habitat opportunities. There are strong contrasts between the ability to succeed in the ¢eld on generalised, open, but strongly limited terrains versus (at the extreme opposite) within exuberant mature mesic forest vegetation. These contrasts emphasise the roles of physical/chemical versus biotic pressures with which respective pteridophytes are confronted. Mature forest vegetation, and especially rain- forest, is widely appreciated to be a very complex community, within which niche preferences be- tween fern species are almost certainly very pre- cisely and exactingly di¡erentiated (e.g. Page, 1979b, 1988; Petersen, 1985; Cousens et al., 1988; Young and Leon, 1989; Van der Wer¡, 1992; Tuomisto and Ruokolainen, 1994; Poulsen and Neilsen, 1995; Poulsen and Tuomisto, 1996; Tuomisto and Poulsen, 1996). Most pteridophyte species from such sources can be successfully reared in glasshouse culture (personal observa- tions 1958^2001) on relatively arbitrary standard-

ised horticultural compost media (including, ironically, most epiphytes, providing that they are not over-fed with standard nutrient additives). This indicates that the often high localisation of forest species in the ¢eld is not purely (or even mainly) the result of narrow mineral tolerances and speci¢cities (beyond the general one of epi- phytes). Instead, the niche-width of these in the wild (often extremely narrow, sometimes also highly localised) is mainly prescribed by overrid- ing interactions of immeasurably subtle, complex, and highly pervasive, biotic competition. By contrast, ability to succeed on more gener- alised terrains with lowered (or initially virtually zero) biotic competition can open wide habitat opportunity for those species which are able to achieve high tolerance levels of the ruling nutrient disequilibriums. For these, the edaphic speci¢city can seem very high. Yet many pteridophytes which are vigorous (sometimes to the extent of being rampant) in edaphically low-nutrient habi- tats in the wild (notably, for example, many Ly- copodiaceae, virtually the whole of the Gleiche- niaceae and Lindsaceae, Dipteridaceae, Matonia and Christensenia, and most Schizaeaceae) can, ironically, prove extraordinarily di⁄cult to grow at all in conditions of experimental cultivation! Extremely high and exacting directly edaphically limited tolerances and limitations seem indicated for such pteridophytes. Both suites of this nutrient disequilibrium tol- erance strategy, either separately or in combina- tion, advantage ferns in enabling them to grow in a wide range of sites which are either too nutrient- poor or are too high and toxic in unusual (e.g. metalliferous) elements for most other competi- tors to succeed equally well. The net e¡ect of these abilities is to open a variety of low-competi- tion habitat opportunities for colonisation into sites which can be widely available to pterido- phytes because of the migratory e⁄ciency of the airborne spore (see Section 3.5: High migrational ability of the airborne spore). Typical habitat ex- amples include:

b intrinsically nutrient poor sandy heathlands and savannahs;

b the leached soils of constant light rainfall conditions such as laterites and those of mountain

C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33


saddles where conditions of constant downward water and nutrient movement apply (e.g. Dipteris, Plate II, 5);

usual degrees of tolerance levels from both suites, and the levels of such tolerances often appear to

be highly taxon-speci¢c. A smaller diversity of


newly formed volcanic ash surfaces;

plant habits is present, with plants usually of


post-wild¢re sites;

small size, scattered (seldom contiguous) occur-

erosion surfaces of lithophytic sites; b habitats of high metalliferous availability such as ultrama¢c soils and man-made metallifer- ous mine spoils;


rence, and tough, leathery growth. Dead fronds, frond debris and especially frond bases may per- sist around parent plants for years. On directly nutrient poor edaphic sites, either characterised

epiphytic habitats. Wide arrays of fern species from diverse fami- lies are today specialist colonists of many of these sites, with considerable specialisations especially of life-form between di¡erent fern families in ex- ploiting di¡erences between each of these rela- tively demanding situations. For example, epiphytic habitats almost exclu- sively require unusually high tolerance levels of the low-nutrition suite, and subtle levels of biotic competition are probably also involved in di¡er- entiating between di¡erent ‘preferred’ epiphytic substrates. Despite these limitations, an enormous number of pteridophyte (especially fern) epiphyte species exist. Some (e.g. species of Tmesipteris) are themselves specialists mainly of tree-fern trunks, even to genus (Dicksonia), while the majority even specialise in the occupation of speci¢c branch niche locations (often prescribed by their mor- phology) and tree canopy heights occupied on particular tree species hosts. The whole epiphytic pteridophyte suite is composed of an enormous range of morphological habits of pteridophytes, from creeping to pendulous, and some quite bi- zarre compost-making specialists. Many can to- tally blanket portions of the bark of the tree on which they grow. Some appear physically inter- dependent, and some are symbiotically ant-asso- ciated in obligate or facultative ways, or subse- quently form various other animal and other pte- ridophyte habitats. Typically they are (relatively) fast-growers, and the duration of life of all as a maximum is limited to that of the tree on which they grow. Many fall in storms, often driven by their own weight, where they die and decompose rapidly on the forest £oor, due to combinations of construction of many soft and semi-succulent parts as a consequence of their growth rates. By contrast, ultrama¢c sites clearly require un-


by post-¢reburn environments or (especially) by erosion-regimes and constant surface moisture downwash such as today on high-mountain sad- dles, notably sprawling and often rampant pteri- dophyte habits are especially characteristic, with tough growth structure typically yielding much local and outwash debris. The frequency of occurrence, and the taxonom- ic diversity, of ferns in all of these habitats today, with subtle di¡erences between sometimes related taxa and their adaptations, suggests a long past history for this phenomenon. Sites of unusual mineral availability must have always occurred, while ¢reburn sites, some with ferns, are known since at least the Early Carboniferous (¢de Scott and Jones, 1994; Falcon-Lang, 1998, 1999; DiMi- chele and Phillips, 2002-this issue). Volcanic ash habitats, also with ferns, are known from at least similar times (Scott and Galtier, 1985; Brous- miche et al., 1992; Crowley et al., 1994). The antiquity of this strategy, which probably enabled opportunistic colonisation even among early ¢li- caleans, is further indicated by Galtier and Phil- lips (1996). Epiphytism amongst ferns, although very fragmentarily known (e.g. Sahni, 1931; Rothwell, 1991; Poole and Page, 2000) has a very long fossil history from the Palaeozoic (Ro« ss- ler, 2000; DiMichele and Phillips, 2002-this issue). Survival of ancient biota collectively on such sites seems also indicated amongst extant taxa by the occurrence of taxonomically outlying and presumed relictual species of ferns associated with apparently relictual conifers as enclaves on some heavily mineralised soils. One example is the oc- currence of several Schizea species and the mono- typic Stromatopteris moniliformis closely co-asso- ciating on ultrama¢c soils in New Caledonia (Page, 2002a,b). The exploitation of the ability to colonise a variety of low nutrient habitats is


C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33

a strategy which is probably widespread through

the fossil record for Pteridophyta, and doubtless has included, within its exponents, many di¡erent groups of ferns. Many terrestrial ferns as far back as the Early Carboniferous have ‘sprawling’ or ‘rampant’ habits (DiMichele and Phillips, 2002- this issue) and one cannot help but note that this habit is characteristic of extant pteridophytes surviving on the poorest edaphic terrains.

3.5. High migrational ability of the airborne spore

The dispersal potential of the airborne pterido- phyte spore confers on ferns the potential of un- usually high dispersal mobility. Main advantages arising from this appear to be:

(1) potential to continually arrive at sites of poor access, such as rock-faces and, especially,

epiphytic sites; (2) potential to arrive rapidly at newly arising locations and thus pioneer habitats, such as land- slide surfaces and new volcanic terrains; (3) potential to achieve (however occasional) long-distance dispersal, from continents to ocean-

ic islands or between remote island chains.

These potentials are not mutually exclusive, and all possible combinations of one, two or all three are clearly available. Furthermore, all are not

once-only events, but apply continuously to spore generation and release processes in most fern communities. All spore dispersal achievements are described here as ‘potential’ since to what degree they are

actually realised in nature is clearly complex and

is yet only fragmentarily understood. Many var-

iations in circumstances must apply. Exactly how signi¢cant long-distance dispersal might be in pteridophytes has, for example, long been a topic of debate (e.g. Gregory, 1945; Lloyd, 1974a,b; Parris, 1985; R.M. Tryon, 1985, 1986; Kendall et al., 1986; Lacey and McCartney, 1994; Caul- ton et al., 1995; Schneller, 1996b), though there are few exacting data on this issue. My own interpretations are based on three lines of evidence: (1) my personal ¢eld experience of fern £oras on oceanic islands in three major oceans today; (2) the known longevity of wide taxonomic arrays of fern spores in captive storage

(4^25 yr in packets, a maximum of 63 yr recorded on an herbarium sheet); and (3) the known resis- tance of fern spores to environmental hazards (see Page, 1979b for an earlier review). These interpre- tations, however, equate closely with those de- rived by Cousens (e.g. Cousens et al., 1985, and personal communications 1980^1986), also based on independent experimental studies and parallel ¢eld observations, which included the appearance of taxonomically novel pteridophytes along the American Gulf Coast following episodes of hurri- cane damage. I take a pragmatic approach and simply begin from the practical stand-point that all fern spores have, and always have had, oppor- tunity to get more-or-less everywhere given time. Sure, there will be a very rapid gradient of spore density dilution away from the parent plant. However, spores can also disperse in long and steady smoke-like plumes, and once airborne, can enjoy great resistance to known environmen- tal hazards (see Section 3.6: Spore tolerance of adverse aerial environments). I conclude that it is not dispersal per se that is usually limiting in terms of achievement of dispersal potentials in pteridophytes (and that endless discussion of fern-spore migration abilities is a red-herring in terms of dispersal usually achieved). Instead, it is the opportunities for establishment of arriving spores, against indigenous biotic competition, that is the real issue determining and confronting eco- logical achievement and ultimate range: create the appropriate habitat, and the appropriate pterido- phyte coloniser will, sooner or later, appear there. The likely e¡ect of distance is usually to in£uence the timing, rather than the actuality, of the event. In this, disturbance regimes especially promote renewed colonisation opportunities, almost irre- spective of where located, and biologically it is probably those few spores that actually do get far that are the real ecological and evolutionary achievers. Some genetic evidence, which appears to sup- port these views, has been recently gained in the case of the rare fern Dryopteris remota (Schneller et al., 1998). Furthermore, the activeness of many pteridophyte discharge mechanisms would appear to have evolved particularly in response to selec- tion pressures to optimise high mobility gain,

C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33


rather than to fall near to the parent plant. Addi- tionally, as pointed out long-ago by Manton (1950), a single spore arriving by long-distance dispersal must self fertilise if it is to establish a ¢rst colonising sporophyte. Most ferns appear to have this potential (see Section 3.7: Flexibility of breeding systems to match varying ecological op- portunity). A genetic consequence of this is, of course, that restoration of the diploid chromo- some number ensures that every gene becomes homozygous and thus phenotypically expressed in the new sporophyte, irrespective of whether that gene was recessive or dominant in the pre- vious population. The haploid propagule thus en- sures that long-distance originating founder pop- ulations can arise which are immediately di¡erent in detailed adaptation to those of their previous population, and on which natural selection for that location at that time can consequently oper- ate. This would seem to be particularly signi¢cant both today and through geological time in the evolution of the fern £oras of remote sites, and especially those of oceanic islands. The dispersal facility conferred by the airborne spore, creating an ever-present unseen ‘spore- rain’, is clearly a powerful and constantly recur- ring factor in pteridophyte ecology (Page, 1967a, 1986), and undoubtedly must have likewise have been so virtually throughout the history of land plants. In combination with some of the above tolerances, perhaps the most spectacular palaeo- examples of the ‘spore-rain’ potential have been rapid achievement of ‘fern-spikes’ following the great environmental disturbance events of the Cretaceous^Tertiary and perhaps also the Trias- sic^Jurassic boundaries (e.g. Spicer, 1989; Fowell and Olsen, 1993; Srivastava, 1994; and see also Collinson, 1996, 2002-this issue, for discussion).

3.6. Spore tolerance of adverse aerial environments

Virtually all of the potentials outlined above would be negated if the fern spore was not viable on arrival at a potential germination site. Long distance dispersal may involve exposure to a range of aerial extremes en route, including those of extreme dryness, cold temperatures and irradi- ation. Much of the earlier data on this topic (see

Page, 1979b) still remains valid. This leads to the view that ferns spores are highly resistant to vir- tually all of the conditions which they might be expected to meet during the course of airborne dispersal, even were this to be prolonged and at high altitude. Additional aspects of spore viability-persistence in the ¢eld in relation to soil spore banking have also recently been discovered in ferns (Dyer and Lindsay, 1992, 1996; Lindsay et al., 1994). Schneller (1996b) has further shown an important contribution by banked spores in helping to achieve a potential, when exhumed, of forming many di¡erent genotypes at any location within the population’s area. Furthermore, there is great diversity in the architecture of fern spores (see, for example, the many excellent illustrations of Tryon and Tryon, 1982), yet almost nothing is known about the adaptive and ecological signi¢cance of their varying morphological characteristics. Some discussion of possible functional roles of spore ornamentation including in resistance and disper- sal, is given by Kramer (1977); A.F. Tryon (1986) and Van U¡elen (1986) and by Hemsley et al. (1999) ^ mainly on megaspores. Another result of extended spore viability is the ability conferred for migration and e¡ective long- distance dispersal. The typically high proportions of Pteridophyta in the £oras of oceanic islands (see Section 3.5: High migrational ability of the airborne spore), demonstrate the e⁄cacy of this, and may well have been one of the main selection pressures for achievement of such viability poten- tials. Floristic patterns between such areas in the fossil record could well provide valuable indica- tors of the progress of evolution of such achieve- ment. [A review of Mesozoic, Cainozoic and mod- ern fern biogeography (Moran, 2001) will provide a basis for future study of this topic.]

3.7. Flexibility of breeding systems to match varying ecological opportunity

In addition to direct ecological achievements shown by pteridophytes, relatively complex breed- ing systems exist which play important roles in endowing these plants with £exibility to con- stantly respond to environmental challenges. Three


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mating-system patterns are generally recognised in ferns: sel¢ng (1) within or (2) between prothalli of the same parent sporophyte (intragametophytic and intergametophytic sel¢ng, respectively) and (3) outcrossing between prothalli arising from the spores of di¡erent parent sporophytes (inter- gametophytic crossing) (Klekowski, 1972a,b, 1973a,b, 1979, 1982; Soltis and Soltis, 1987, 1992). While mating between prothalli, whether these be from the same parent sporophyte or from dif- ferent parent sporophytes, is clearly obligate in hetersporous ferns, in the majority of living ferns (which are homosporous) mating-systems are to a high degree £exible and opportunistic. The pro- thalli of homosporous ferns have, in general, both male (antherdial) and female (archegonial) or- gans. There is normally a time-phase di¡erentia- tion between maturity of the organs of the two sexes. However, there may also be a period of overlap, and for most taxa, so far as is known, either intragametophytic and intergametophytic sel¢ng can be an option only if out-fertilisation by intergametophytic crossing fails. Outcrossing is thus likely to be e¡ectively realised wherever appropriate opportunity arises, and, with certain limitations (Schneller, 1996a), most ferns are widely regarded as being extreme outcrossers, with only a few nearly exclusively inbreeders known (e.g. Ranker, 1992; Soltis and Soltis, 1992). Where whole populations of prothalli exist, then sexual balances amongst prothalli growing from homosporous spores are known to be fur- ther mediated by antheridiogens (e.g. Schneller et al., 1990; Korpelainen, 1997), the in£uence of which further encourages outcrossing and mini- mises sel¢ng. In wild prothallial populations, the e¡ects of such antheridiogens can be enhancement of the reproductive success of small gametophytes through promotion of gender expressions, which would not necessarily otherwise occur (Hamilton and Lloyd, 1991). The e¡ects of antheridiogens can operate between prothalli of di¡erent species in establishment of contrasting sexuality. This is probably one of the factors promoting the num- ber of independent congeneric hybrids which have been ¢eld-recorded in pteridophytes (see Rothmaler, 1944; Wagner, 1954; Walker, 1958; Duckett and Page, 1975; Page and Barker, 1985;

Wagner and Wagner, 1985; Barrington, 1985; Barrington et al., 1989; Page, 1990a,b, 1997b for reviews). Thus, in addition to examples of ecological in- £uences, we also need to lookat breeding systems. These genetic potentials have probably become increasingly varied and sophisticated through evo- lutionary time. Nevertheless, many must be an- cient in their basic origins and e¡ects, helping to underpin a great diversity of fern ecological achievements throughout the fossil record. As with phytochemical armament (see above), there is much workyet needed in drawing comparisons between the breeding systems of more primitive and more advanced living taxa and setting this against the known fossil history and ecologies of the groups concerned.

3.8. Revivalist tendencies of certain gametophytes

In an experiment carried out by the author (Page, 1967b), prothalli of a range of mediterra- nean-climate ferns of the genera Notholaena and Cheilanthes (Sinopteridaceae) (originating from the Canary Islands) which were tested on an ex- ploratory basis, showed exceptional abilities to withstand complete desiccation for enduring peri- ods. Such desiccated prothalli were successfully rejuvenated from a ‘crisp and dry’ completely air-dry state after storage for many months, by eventual return of overhead application of free water, imitating rain. Not all cellular sectors of each individual pro- thallus necessarily survived such treatment, but enough green tissue persisted in most to act as ‘revival centres’ from which new growth resumed, and from which complete new prothalli with new sex organs then grew. Indeed, frequently more than a single such centre persisted in single pro- thallus, with the result that two or more new pro- thalli resulted where there was formerly only one. Sexual maturity then followed, with the origin of a completely new ‘replacement’ generation of sporophytes. This contrasted with the young spo- rophytes of the same taxa arising from them, which so far as my own observations have shown, have no comparable desiccation recovery abilities. This glasshouse experiment con¢rmed earlier

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observations made independently on di¡erent spe- cies by Pickett (1914). However, the existence of this ability in ferns appears to have been little appreciated and I am not aware of any other studies that have been made since. The lackof extensive experiment across a broad taxonomic and habitat basis means that the extent of this ability of pteridophyte gametophytes is unknown. This is, however, a strategy in ferns which could have far-reaching potentials in opening cer- tain habitats for a range of taxa today, and which may well have been of signi¢cance in the past. Prothalli could succeed under moisture regimes which are intermittent and unpredictable, on a ‘try and try again’ basis after an initial prothallial foothold has been successfully gained. Such pat- terns of survival could be advantageous in a num- ber of di¡erent habitats, varying from sub-desert sites to rockface habitats and even epiphytic ones. In this behaviour, fern prothalli of a range of genera are displaying a similar, if unexpected, behaviour to mosses, suggesting that it could well have relevance for the processes of fern-colonisa- tion even in apparently hostile conditions, both today and in the past.

potentials of polyploidy). Main achievements of sporophyte longevity are:

(1) capitalisation on success of achievement of the gametophyte stage and subsequent physical retention of a hard-won niche; (2) that maximisation of sporophyte size can be achieved: this is important, for example, in gain- ing frond size exposure to most dispersive air-cur- rent opportunities; (3) spread of spore output of genetically suc- cessful individuals over the longest number of years: this is of particular advantage, for example, in achieving successful colonisation of habitats which appear only sporadically. Assessments of longevity in fossil pteridophytes in relation to past selection pressures in di¡erent environments would be valuable. However, it is very di⁄cult to establish fern longevity in the fos- sil record (Collinson, personal communication, 2001). One has to presume that tree ferns espe- cially must always have been long lived and that, amongst other Pteridophyta, horsetails must have been similarly so. Therefore, amongst the giant Carboniferous representatives of these plants sporophyte longevity was probably the norm.

3.9. Potential longevity of resultant sporophytes

3.10. Exploitation of mycotrophy

An often overlooked advantaging strategy, sporophyte longevity, may well be a particular feature of more ancient plants. It is also widely present in extant conifers (Page, 2002a,b), and here too relatively especially so amongst many more ancient members. In ferns, examples of sporophyte longevity include tree ferns from 150 to 200 years (e.g. in cultivation at PenjerrickGar- den in Cornwall) and Osmunda plants said to be up to 300 years old in cultivation. In the wild, the rhizomatous fern Platyzoma is estimated to be about 500 years old based on growth rates of 2^ 3 mm per year and the diameter of the ‘fairy ring’ it had formed (Page, personal observations). Drawbacks of vegetative longevity are perhaps that, in contrast to species with rapid life-cycle turnovers, rates of adaptive change are committed to be slow. Slow life-cycle turnover may have con- tributed to evolutionary stasis seen in several pteri- dophyte groups (see Section 3.11: Exploitation of

Mycorrhizae have been widely recorded in as- sociation with the roots of extant ferns in ¢eld surveys in widely scattered locations (e.g. Burge¡, 1938; Cooper, 1976; Iqbal et al., 1981; Newmann and Reddell, 1987; Jones and She⁄eld, 1988; Gemma et al., 1992; Moteetee et al., 1996). This suggests that such associations may well be a nor- mal feature of the roots of the majority of extant ferns as well as ancient pteridophytes (Pirozynski, 1981, 1988; Taylor, 1990). As a generalisation, there appears to be an emerging picture that my- cotrophy, though frequently present in the ¢eld gametophyte and sporophyte generations, is more obligate in more primitive (especially eusporan- giate) taxa (e.g. Montgomery, 1990), and prob- ably more facultative in most more advanced (especially leptosporangiate) genera. This is sup- ported by observations from experimental culture which indicate that gametophytes of virtually all leptosporangiate taxa tested will grow successfully


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aseptically, but there are other claims that ‘best’ growth is achieved when prothalli have access to normal soil fungi (e.g. Hutchinson and Fahm, 1958). Where associations are facultative, it would seem most likely that these could most advantage ferns either in terms of growth, perranation or in achieving exploitation of unusual and perhaps ex- acting ecological habitats, but remarkably little is known about this. By complete contrast to ferns,

I know of no reports of mycotrophy in horsetails,

though experiments I have carried out growing roots of Equisetum in aqueous culture (Page, 1967b) show that the sporophyte itself has long and unusually persistent root hairs, which may well function in a similar manner. Mycotrophy in pteridophytes is signi¢cant, however, in that it would appear to be of partic- ularly ancient occurrence in primitive land plants since at least the Early Devonian (e.g. Taylor, 1990; Banks and Colthart, 1993). Data linking between past pteridophyte diversity and exploita- tion of mycotrophy would be valuable, since such relationships may well have provided a particu- larly important advantaging strategy for fern suc- cess in a wide array of habitats throughout geo- logical time.

3.11. Exploitation of potentials of polyploidy

The contribution which the exploitation of the potentials of polyploidy (and especially allopoly- ploidy) has made to the achievement of speciation in ferns has been one of the main areas of new understanding in this group in the last 50 years (e.g. Manton, 1950; Shivas, 1961; Walker, 1958, 1966a,b, 1979, 1985; Page, 1967b, 1973, 1997a;

Lovis, 1977; Wagner and Wagner, 1980; Werth et al., 1985; Soltis and Soltis, 1987; Barrington et al., 1989; Hau£er, 1989a,b, 1992; Wolf et al., 1990, 1991; Rabe and Hau£er, 1992; Hau£er et al., 1995). It has become clear that while autopo- lyploidy is only an occasionally successful evolu- tionary route in ferns, allopolyploidy is widely successful (Walker, 1979, 1985; Hau£er, 1996). Allopolyploidy allows for existing genomes to be recombined in new and fertile taxa. It provides

a rapid route for species evolution and adaptation

in ferns, and, where most successful, it tends to

produce plants of enhanced vigour, typically re- £ected in increased size and/or faster vegetative growth rates. Ferns have large numbers of small chromosomes in cells with high cytoplasmic vol- ume ratios. This enables many stages of chromo- some doubling to be successively accommodated upon one another, while maintaining full opera- tional integrity of the cells themselves during their crucial mitotic and meiotic divisional processes. Allopolyploid-derived tetraploids, octoploids and ploidy levels up to 16 ploid are known, and may be higher than this in some genera whose base numbers are uncertain. Back-cross hybridisations, between members of di¡erent ploidy levels within genera, appear to be just as common as crosses between those of the same level. The permutations which can result are many, progressively building complex reticulations of inter-speci¢c relation- ships within individual genera (e.g. Wagner, 1954; Hau£er and Windham, 1991; Hau£er et al., 1995; Thomson, 2000). Additional outcomes in terms of fern genetic potentials, which may be related to ploidy levels, include the existence of hybrid swarms (¢rst pro- posed in Pteris by Walker (1958) and recently con¢rmed by molecular work, for example in Po- lystichum ^ Mullenniex et al. (1998). In addition there are multiple hybrids at the same ploidy lev- el, some of which produce a percentage of appar- ently good spores (Page, 1963, 1990a, 1997b). A mechanism for stabilisation of hybrid reproduc- tion at a homoploid level, autogamous allohomo- ploidy, has also been proposed (Conant and Cooper-Driver, 1980). Opportunity also exists for changes in mating systems, high genetic heter- ozygosity, the survival of genetic redundancy and the ability for species, including narrow endemics, to store high genetic variability (e.g. Chapman et al., 1979; Gastony and Gottlieb, 1982). Also an initially limited gene pool of an allopolyploid may be enriched as a result of multiple origins, muta- tions and/or intergenomic recombinations (Werth, 1992). In established polyploids, silencing of du- plicate gene expressions (Werth and Windham, 1991; Gastony, 1991) and practical genetic dip- loidisation may subsequently ensue (e.g. Wolf et al., 1987, 1990). The whole process results in the creation of morphological and ecological novelty,

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genetic diversity, maintenance of fertility, and clear separation of genetic identity between dip- loid progenitors and polyploid derivatives. The practical evolutionarily results are:

(1) the speed with which new taxa of ferns can arise as pure-breeding lines; (2) that resultant ‘instant’ taxa are each adapted to somewhat di¡erent ecological conditions than the parental taxa; and (3) that such new taxa may combine new eco- logical abilities with hybrid vigour. In consequence, in long-stable environments, it is likely that allopolyploids, though they may arise, will be seldom necessarily more successful than their parents if these are already ecologically well-adapted. However, in more actively evolving £oras and under more changing environments, higher ploidy derivatives can more often ¢nd niches clear for ecological success, probably even- tually displacing many of the original ancestral diploids. An extreme range of contrasts amongst fern ploidy spectra is thus apparent. The long-sta- ble and highly encapsulated fern £ora of the Can- ary Islands has well under 30% polyploidy and these only of low ploidy grades (Page, 1967b, 1973). This can be compared with the less con- ¢ned and more actively evolving fern £oras of either post-Pleistocene deglaciated areas of Eu- rope (e.g. Manton, 1950; Vogel et al., 1998). or with what have been widely regarded as more modern tropical fern £oras (e.g. Jamaica and Tri- nidad ^ Jermy and Walker, 1985; Walker, 1966a, 1985). In these examples, over 70% polyploid rep- resentation, including high grades of ploidy, is more typical. The former circumstances thus have the greatest possibility of preserving relictual taxa in ferns (with many of the ferns of the Can- ary Islands, for example, surviving today little changed since the Miocene ^ Page, 1967b), the latter for the success of much newer diversity. Even if only some of these aspects have applied throughout the past history of ferns the potential conferred on ferns to meet new environmental challenges is clearly high. These mechanisms may well have contributed signi¢cantly and sub- stantially to fern ecological adaptive change and hence long-term fern survival and diversi¢cation. Evolutionary stasis, perhaps in part involving

ploidy stability and in part related to life-cycle longevity, has been identi¢ed in several genera and species groups within the fossil record (e.g. Rothwell and Stockey, 1991; Delevoryas et al., 1992; Rothwell, 1996a; Herendeen and Skog, 1998; Phipps et al., 1998; McIver and Basinger, 1989; Serbet and Rothwell, 1999; Pigg and Roth- well, 2001). High polyploids may be typical of past activity in some ancient lineages, such as Ophioglossum and Equisetum, while mechanisms are also provided whereby opportunities for new developments from old stocks (e.g. Page and Barker, 1985; Ollgaard, 1992) can also rapidly occur.

3.12. Biotic independence

Apart from mycorrhizal associations (see Sec- tion 3.10: Exploitation of mycotrophy), and cer- tain known examples (e.g. the genera Lecanopte- ris, Solanopteris, Pteridium) where ferns gain additional protection of their whole vegetative structure by attracting ants (see Section 3.2: Di- verse phytochemical armament), there are few other pteridophyte^animal associations. The only ones of which I am aware, are the spiny spores in some Isoetes species (e.g. I. echinospora) which appear to be an adaptation to bird dispersal (Page, 1982b). Also some echinate spores, and the unusual lasoo-like ¢lamentous outgrowths of spore walls in Lecanopteris mirabilis, have been suggested to be an adaptation to spore transport by the sporophyte’s associated ants (A.F. Tryon, 1985, 1986). It is, however, noteworthy that only a very few known examples exist and a certain level of quite local evolutionary experiment seems indicated, with methodologies which, in pterido- phytes generally, appear not to have become widespread. Throughout the vast bulkof pteridophyte di- versity, there appears to be remarkably little de- pendence on animals in general achievement of the main life-cycle functions of vegetative growth, propagule dispersal or sexual achievement. Most ferns consequently constantly ‘shun’ rather than ‘court’ most animal species. This is in great con- trast especially to the £owering plants, where courting of animals (especially of pollinating in-


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sects by £owers) has enabled often complex and sometimes bizarre pathways of achievement to evolve which are presumably more e¡ective than could be achieved without such support. Two important advantages accrue, however, for ferns:

(1) Having established e¡ective pathways of biochemical defence mechanisms (see Section 3.2: Diverse phytochemical armament), there is an uncomplicating freedom to apply these without limitation throughout all the varied stages of the plant life cycle. (2) It has enabled the main life processes of Pteridophyta, including dispersal and mating, to be achieved virtually exclusively with the presence of the simple physical agencies, which change lit- tle with time. Any partitioning of toxic e¡ects from certain organs or life-cycle stages is thus clearly unneces- sary if animals do not need to be courted. This has contributed enormously to the fern’s freedom of specialisation in defence through the develop- ment of whole cocktails of diverse chemical agents, against which animal groups are least likely to evolve complete defences. For example, in combination with other agents, the production of insect ecdysones by ferns must be a defence to which it is di⁄cult for an insect to evolve resis- tance, even through geological time! Such biotic independence today almost cer- tainly closely re£ects a life-style which probably began with the ¢rst vascular land colonisers. Thereafter, through the dependence for dispersal and reproduction solely on only uncomplicated physical agencies pteridophytes have audaciously, solidly and unambiguously ‘pinned their colours’ to those agencies which neither change signi¢- cantly through time, nor become extinct. Such in- dependence has contributed signi¢cantly to what these plants have been able to achieve, and con- sequently to the close comparability between modern and fossil pteridophyte life-styles.

4. Discussion and conclusions

Very considerable pteridophyte ecological di- versity survives today (Copeland, 1907; Holttum,

1938, 1954; Page, 1977, 1979a,b; Page and Clif- ford, 1981; Johns, 1985), with over 12 000 species of ferns alone. In terms of species richness, homo- sporous pteridophytes are more successful than all other non-angiosperm grades combined (Roth- well, 1996a). This account demonstrates that, amongst pteridophytes, similar general responses are shown time and time again by distantly re- lated taxonomic groups in response to similar se- lection pressures. Using knowledge of the ecology (especially autecology, life-cycle biology, environ- mental interrelationships and adaptations) of ferns and fern allies today, an attempt is made to analyse why pteridophytes are able to colonise such a range of habitats, and especially so many marginal ones. This synthesis is used to derive basic principles concerning the innate biological weaknesses (limitations) and special strengths (ad- vantages) of Pteridophyta as a whole, which are presented here. The seven limitations identi¢ed are innate weaknesses of pteridophytes, which clearly limit fern potentials and achievements today. Clearly, none of these have been able to be successfully ‘thrown-o¡’, to any major degree, in the course of pteridophyte evolution. On this evidence, all must have acted as similar limitations throughout pteridophyte evolutionary history. Interestingly, few of these (perhaps only the single growing point (Section 2.2: Single growing-point limita- tions of sporophyte architecture)) might be de- duced directly from the fossil record itself, and most would therefore be unknown if we did not have evidence from the living plants. By direct contrast, the 12 advantages conserva- tively identi¢ed (14 if including subcategories within Section 3.2: Diverse phytochemical arma- ment, and Section 3.4: High tolerance of acute nutrient disequilibrium substrates) clearly open opportunity for exploitation of a considerable ar- ray of ecological habitats by pteridophytes today. Many have the ability to operate in varying de- gree, with a range of subtle variations in e¡ect. Virtually all have the potential to operate in com- binations, helping to explain the ecological diver- sity which pteridophytes, and especially ferns, have achieved. Experimental evidence indicates that most of these advantages appear broadly

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across most taxonomic groups and seem to have deep-rooted origins within Pteridophyta, to the degree that many are judged to be special innate abilities of these plants. On this evidence too, most must have also been available to operate throughout pteridophyte evolutionary history. Some, such as tolerance of extremes of edaphic conditions, may have actually directly helped sur- vival of several ancient fern genera to occur (Page, 2002d). Interestingly again, a few might be proven, some others inferred, but many would also remain unknown, especially in the potentials which they liberate, if we did not have evidence from the living plants. The 12 advantages help to mitigate, to tolerate, and sometimes to positively exploit, the worst ef- fects of the seven limitations in a number of ways. For example, the handicap of an independent ga- metophyte stage, the poorly controlled evapora- tive potential, and the need to ‘return to the water to breed’ are all to a degree o¡set by the abilities conferred by high disease resistance under satu- rated humidity levels. Upon this balance, low- light photosynthetic abilities then enable many such high-humidity but necessarily low-illumina- tion habitats, in which biotic competition levels are generally low, to become exploited to the full. Slow plant growth rates may be less of a handicap under these often most stable of condi- tions, while mycotrophic exploitation in gameto- phyte and sporophyte generations doubtless fur- ther supports survival in these and many other marginal habitats. Intolerance of widely £uctuat- ing conditions by the sporophyte is, in appropri- ate habitats, partly o¡set by the revivalist tenden- cies of certain gametophytes. The single growing- point limitations of sporophyte architecture are partly o¡set by many speci¢c morphological adaptations of genera. These are augmented fur- ther by ecological escapism of many ferns to hab- itats which are either too remote (e.g. epiphytic) or too toxic (e.g. heavily mineralised substrates) for plant and animal pressures to be intense. These habitat opportunities are especially pro- moted by the unusual tolerance levels of ferns for sites of acute nutrient disequilibrium as well as the access to these regularly gained by the high mobility of the airborne spore. Animal browsing

is also targeted by the diverse phytochemical ar- mament of pteridophytes, which has a broad spectrum of e¡ects on animals, especially against invertebrates. Uncontrolled high reproductive commitment, although doubtless a highly en- ergy-intensive process, is combined with potential longevity of resultant sporophytes. Together these attributes are e¡ectively exploited by the high mi- grational ability ( = potential dispersal) of the air- borne spore, coupled with the known spore toler- ances to adverse environmental circumstances. The breeding systems and their diversity are clearly consequent on dispersal opportunities, no- tably the facultative inbreeding fallbackwhen outbreeding fails which enables e¡ective long dis- tance dispersal by a single spore. Today pterido- phyta also gain ecological adaptation and evolu- tionary advantage from their extensive exploitation of potentials of polyploidy (especially allopolyploid progression) and their high degree of biotic independence. It is inferred that these are also attributes with a long past history. Amongst living pteridophytes, ancient elements as well as modern elements often co-exist (Stewart and Rothwell, 1993). Many fern families, notably Marattiaceae, Osmundaceae, Schizaeaceae, Glei- cheniaceae, Matoniaceae, Dipteridaceae, Dick- soniaceae, Cyatheaceae, Azollaceae, Salviniaceae and Marsileaceae, have well established, extensive fossil records (Collinson, 1992, 1996, 2002-this is- sue; DiMichele and Phillips, 2002-this issue; Van Konijnenberg-van Cittert, 2002-this issue). Other non-fern pteridophytes, especially Equisetaceae (Page, 1972a,b), Selaginellaceae (Page, 1989) and Lycopodiaceae (Wikstro« m et al., 1999) show evi- dence of adaptive traits which must also have oc- curred in the past biology, ecology and ancient morphologies of these groups. Periods of evolu- tionary stasis have been recognised, either from the fossil record of single species such as those of Osmunda, Onoclea and Woodwardia (e.g. Roth- well and Stockey, 1991; Rothwell, 1996a; Phipps et al., 1998; Serbet and Rothwell, 1999; Pigg and Rothwell, 2001), or in whole pteridophyte £oras from their surviving cytology (Page, 1967b, 1973). Similarly, there may be little change in at least some generic a⁄nities with habitats through time. Examples certainly include Onoclea, Osmun-


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da and Woodwardia, which appear to have had members associated closely with swamp habitat margins similar to those of today since the Ter- tiary or earlier (e.g. Rothwell and Stockey, 1991; Greenwood and Basinger, 1994; Pigg and Roth- well, 2001; Collinson, 2002-this issue); Equisetum with similar habitats for at least as long (McIver and Basinger, 1989) or very much longer (Page, 1967b, 1972a); Acrostichum, characteristic today of (uniquely) humid-tropical brackish-water es- tuaries and swamps, and spreading into the sea- ward-face of mangrove swamps today, clearly as- sociated with lakes and freshwater marshes in the Cainozoic (Collinson, 2002-this issue); free-£oat- ing water ferns (Azolla and Salvinia) in freshwater facies with a range of associated aquatic angio- sperms widespread in the Cainozoic (Collinson, 2002-this issue); and gleicheniaceous and schi- zaeaceous ferns as opportunists colonising open and disturbed ground including ¢reburn sites and volcanogenic terrains since at least Mid-Cre- taceous (Collinson, 1996, 2002-this issue; Van Konijnenberg-van Cittert, 2002-this issue). More contentious (Collinson, 2002-this issue) at present is the claim (Poole and Page, 2000) of a probable Eocene epiphyte of Polypodiaceous a⁄nity, though I maintain my conviction: if there are Polypodiaceae and there are trees, then there are epiphytes (though I do not dispute that additional evidence of these in physical connection would be valuable!). Fern epiphytes are proven in Palaeo- zoic £oras, attached to tree fern trunks (Ro« ssler, 2000; DiMichele and Phillips, 2002-this issue). The ecology of living pteridophytes shows that this group is both complex and dynamic, and that these complexities still confer great versatility, £exibility and adaptive e¡ectiveness, especially through their abilities of exploiting an unusually wide range of marginal habitat conditions. Ferns have, in consequence, achieved long-term surviv- al, diversi¢cation and success through evolution- ary time. Although primitive forms persist, diver- si¢cation continues to occur on the basis of not only modern stocks (e.g. Wagner, 1954; Hau£er and Windham, 1991; Hau£er et al., 1995) but also on already ancient ones (e.g. Page and Barker, 1985; Page, 1972b, 1990a, 1997b; Ollgaard, 1992, 1996). Great evolutionary £exibility and re-

sponsiveness, organisation and ecology have also been emphasised within the Pteridophyta from a fossil perspective since the Palaeozoic (DiMichele and Phillips, 2002-this issue), and a diversity of habitats has been occupied through the Mesozoic (Van Konijnenberg-van Cittert, 2002-this issue) and Cainozoic (Collinson, 2002-this issue). All of these alternatives will have operated, perhaps with varying emphases and in varying degrees, between times of relative evolutionary quiescence versus periods of more active radiation (Collin- son, 1991, 1996; Rothwell, 1987, 1999). Today their living survivors provide evidence of the diversity of the innate mechanisms and pro- cesses which ferns are able to develop and exploit, and the diversity of adaptations and ecological potentials which can thereby be achieved (Page, 1997a, 2000, 2002c). These same innate mecha- nisms and processes must have similarly occurred throughout much of pteridophyte fossil history, opening similar ranges of adaptations and ecolog- ical potentials, as strategic elements of recurring pteridological achievement. Although drawing comparisons between living Pteridophyta and fossil ones is far from new, most such comparisons have been largely fossil- driven, and relate usually to speci¢c fossil taxa or habitats, seeking their modern equivalents for comparison. Particularly important recent synthe- ses have been made in this perspective by, for example, Rothwell (1987, 1991, 1996a,b, 1999). The approach presented here is proposed as com- plementary to that which can be gained from the fossils themselves. It is argued that the modern fern ecologies help to point to a diversity which could (and probably did) exist in Pteridophyta at many times in the past. Using the same strategies as their modern analogues, ancient ferns, at many di¡erent times and locations, and with both sim- ilar and many di¡erent taxa to those of today, have been similarly enabled to exploit a range of habitat miches as wide as those seen today.


On practical aspects, I am grateful for the support of several generations of horticultural

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staff at the Royal Botanic Garden, Edinburgh, UK, for the day-to-day maintenance of my many pteridophyte and conifer experimental cultures for over more than 30 yr, and those at Oxford, UK, Brisbane, Australia, and Newcastle, UK, Univer- sities for extended periods before this. I am also grateful to the Royal Botanic Gardens, Kew and the Natural History Museum, London, for access to herbarium materials, and to the Linnean Society and Camborne School of Mines, Univer- sity of Exeter, for access to library facilities in their charge. On scientific aspects, discussions in the laboratory, the field and the glasshouse, with Dr. Trevor Walker, Clive Jermy, Dr. Heather McHaf- fie, Dr. Adrian Dyer and Dr. Richard Bateman have been long-term stimuli to the overall devel- opment and progress of these studies and to many of the ideas contained therein. Dr. Heather McHaffie (Edinburgh, UK) has kindly provided additional pteridological comments and Dr. Mi- chael Proctor (Exeter, UK) ecological comments on the resulting manuscript. I am further grateful to Dr. Margaret Collinson for her enthusiasm and support in helping to bring my neobotanical concepts into a palaeo-botanic arena, and to her, Dr. Kathleen B. Pigg and Dr. Paul Kenrickfor many helpful and constructive comments on the resulting manuscript from a palaeo-botanic per- spective. This paper is dedicated to the memory of the late Professor Robert M. Lloyd (Athens, OH, USA), the late Dr. Michael I. Coussens (Pensaco- la, FL, USA) and the late Professor Jan Kornas (Krakow, Poland) all of whom contributed, in discussions and joint fieldwork, to the formation of some of the ideas included here.


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