Ecologivcal Strategies in Fern Evolution[1]

Ecological strategies in fern evolution:a neopteridological overview

Christopher N. Page a;b;�

a Royal Botanic Garden, Edinburgh, UKb Cornwall Geological Museum, Penzance TR18 2QR, UK

Abstract

Drawing inferences about the past from the ecology of living organisms is one of several approaches toreconstructing palaeo-environments. Pteridophytes are a major component of fossil floras, but their use asenvironmental indicators is constrained as much by lack of ecological data on living species as by an understanding ofthe distribution of fossils. Taking a neobotanical perspective, this paper discusses some important ecological strategiesof ferns and allied plants and their underlying selection pressures, based on an extensive survey of tropical andtemperate species and on horticultural experience of the behaviour of wild species in experimental cultivation. Broadlyparallel developments to similar selection pressures and environmental responses have been sought from amongstdistantly related extant families, to derive broad concepts of weaknesses and strengths inherent in the biology of theseplants.From this evidence, seven main limitations and twelve important advantages imposed on pteridophytes by aspects

of their biology are identified as follows:Limitations: b The handicap of an independent gametophyte stage

b Single growing-point limitations of sporophyte architectureb Slow plant growth ratesb Intolerance of widely fluctuating conditionsb Poorly controlled evaporative potentialb Uncontrolled high reproductive commitmentb Need to ‘return to the water to breed’

Advantages: b Low-light photosynthetic abilityb Diverse phytochemical armamentb High disease resistance under saturated humidity levelsb High tolerance of acute nutrient disequilibrium substratesb High migrational ability of the airborne sporeb Spore tolerance of adverse aerial environmentsb Flexibility of breeding systems to match varying ecological opportunityb Revivalist tendencies of certain gametophytesb Potential longevity of resultant sporophytesb Exploitation of mycotrophyb Exploitation of potentials of polyploidyb Biotic independence

0034-6667 / 02 / $ ^ see front matter 8 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

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

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www.elsevier.com/locate/revpalbo

It is argued that collectively these weaknesses and strengths provide a broad framework, which, operating in variedcombinations, limit or open opportunities for exploitation of a considerable array of ecological habitats byPteridophyta. Based on these data, several general ecological principles are developed. It is proposed that, throughtime, such strategies are likely to have opened many pteridophyte habitat opportunities, though not all of these willnecessarily 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 framework of weaknesses and strengthsis likely to have operated in the past, and thus have been of similar relevance in defining and promoting the ecologicalachievements of the fossil pteridophytes in relation to selection pressures and consequent adaptations. This opens upthe 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 fromthe fossil record. 8 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 relationshipsof these plants, we are faced, on the one hand, bya good and very long fossil record through a greatdiversity of global habitats. On the other hand,there are some 12 000 or more living species offerns alone (plus horsetails and clubmosses) in aworld-wide array of extant habitats. Of the livingspecies, we have good world-wide morphological,taxonomic and phylogenetic information bases,but we are only just beginning to ask questionsabout the more subtle aspects of their ecologiesand the reasons behind the adaptations and thearchitectures that we see.In comparing the living and the fossil, it is im-

mediately clear that there is much commonground. However, it is also clear that not everypalaeo-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 necessarilyanswered by the fossil record. Both ¢elds havetheir unique strengths, and provide complementa-ry approaches, between which informationbridges 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 toconstruct a skeleton of ideas and proposals whichcan be tested against evidence. It is then necessaryto 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 toclimatic, and from physiological to genetic andmycological) which need careful evaluation andsensitive interpretation. These data must be re-lated to direct observations of both whole ferncommunities and individual species niches in the¢eld (especially in the wet tropics). Autecologicalinformation is added from life-cycle observationin experimental cultivation. A synthesis of resul-tant data is necessary against the taxonomic spec-trum to which it might apply today, with constantawareness of the areas likely to be of particularpalaeo-relevance. It is also vital to be aware ofwhat is not known or has been inadequatelystudied which, even in living ferns, is manifold.This account focuses particularly on ferns,

although relevant comparable data from otherpteridophyte groups (horsetails and clubmosses)are added where appropriate and available. Theaccount draws on nearly 40 yr of personal ¢eldecological observations and experimental study offerns. Identi¢ed and itemised on the basis on thisevidence are: (1) the intrinsic limitations to fernecological success (Section 2: Intrinsic limitationsto fern ecological success) ; and (2) the importantadvantages imposed on pteridophytes by aspectsof their biology, which establish recurring strat-egies of fern ecology, adaptation and survival(Section 3: The recurring advantaging strategiesof fern ecology, adaptation and survival). These

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enable ferns, despite the limitations, to occupyand succeed in a wide range of ecological nichestoday. An example of this success is the forestmargin 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 examplesof ¢eld situations and responses have been docu-mented from among members of unrelated fernfamilies (both Leptosporangiate and Eusporan-giate) in multiple locations in response to similarselection pressures. This provides a resource-richinformation base, which points to principles ofmodern fern ecological survival abilities whichhave potential to translate into broader palaeo-settings.It is not suggested that all interactions between

fossil ferns and their palaeo-environments havenecessarily 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 underwhich fossil taxa have existed necessarily still ex-ist. Many taxa are also now extinct (DiMicheleand Phillips, 2002). Nevertheless, it is proposedthat similar overall strategies are likely to haveoperated 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 promotedthese.

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 thestrengths of the ecological strategies, which have

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

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

2.1. The handicap of an independent gametophytestage

Restrictions imposed on the sporophyte by theoccurrence, in the life cycle, of an independentgametophyte stage are at least twofold:(1) Collectively, the successful arrival, germina-

tion, and establishment stage provides an ‘achillesheel’ to the whole fern life cycle, and is probablythe stage at which the greatest numbers of indi-viduals (by an order of magnitude) fail and be-come eliminated on a regularly recurring basis inthe ¢eld.(2) Among the few successful establishees, the

resulting gametophyte determines the general siteof 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-livedstages of the fern life cycle, while the process offertilisation itself is also dependent of the addi-tional presence of adequate free-water (see Section2.7: 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 work towards achieve-ment of some degree mutualistic equation of hab-itat tolerance. A few extreme cases are knownwhich serve to show a little of the range of com-plexities which may become involved. These in-clude the occurrence of apogamy, which producessporophytes without fertilisation (Walker, 1979),delayed sex expression (Duran and de la Sota,1996), occurrence of clonal gemmiferous gameto-phytes (Dassler and Farrer, 1996), and occurrenceof pH metamorphosis between gametophyte andsubsequent developing sporophyte in Pteridium(Page, 1986). In ferns with independent gameto-phyte stages, marked contrast exists between theecologies of the gametophyte and sporophyte(Farrar, 1967, 1985; Peck et al., 1990; Rumseyet 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 sporophytesurvival (see also Section 3.11: Exploitation ofpotentials of polyploidy). Such potentials, whichcan be far from ‘textbook’, need to be borne inmind in the interpretation of the breadth of pte-ridophyte adaptation, especially to more unusualpalaeo-habitats.

2.2. Single growing-point limitations of sporophytearchitecture

In great contrast to the multi-growing points ofmany angiosperms, the single growing-point ofthe pteridophyte rhizome (whether it is a terres-trial or aerial ‘stem’) becomes the whole basis forthe origin and direct tenure of not only roots butalso 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 complexphytochemical armament in ferns. (3) Woodwardia radicans thrives on steep ravine sides of dense laurel-forest interiors in theCanary 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 theseconditions. (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 forminggroves 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 newlateral growing points as side-rhizome out-growths, is usually slow. Main avoidance mecha-nisms, which at least partly circumvent this innatevulnerability, include:(1) physical structure: this includes density of

hairs, scales and occasional spines to protect theyoung 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 bysmall- 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 epiphytesamong ferns;(5) high emphasis on biochemical armament ap-

parently e¡ective against a broad-spectrum of an-imal taxa: see Section 3.2: Diverse phytochemicalarmament.In the case of tree ferns, particular vulnerability

then ensues from the creation of a trunk which isitself a desirable habitat for colonisation by otherplants, notably by climbing epiphytes and scram-bling lianes. All of these are harmful to tree fernssince the inevitable upward growth of each isdrawn directly towards the single monopodialtree fern crown. Further architectural develop-ments by the tree fern are needed to counter theseadvances. Two methods are adopted widely byexisting tree ferns. Some produce fast upwardgrowth resulting in a slender trunk which itselfhas a smooth polished surface (with clean frondabscission leaving only smooth leaf scars) uponwhich it is di⁄cult for climbers to gain purchase.Others, such as Dicksonia (Plate II, 1) and somemembers of the Cyatheaceae and Blechnaceae,have slow upward growth (resulting in a thickerand more rough-surfaced root-clad trunk), butthey retain dense ‘skirts’ of old fronds hangingbelow the crowns. These act as a foil to ascendingclimbers and epiphytes which substantially fail to

negotiate round or through this ‘skirt’ (Page andBrownsey, 1986).Such crown vulnerability will have been char-

acteristic of ferns through the whole of the fossilrecord, through which similar (and perhaps other)strategic avoidance mechanisms will have beenelaborated. The presence of either exceptionallyclean trunks to fossil tree ferns or the presenceof persistent tree fern skirts would itself indicatedefensive mechanisms against the presence ofclimbers or epiphytes in the associated palaeo-£ora. It would seem that the Palaeozoic treefern Psaronius used neither of these deterrents ef-fectively as it was colonised by both epiphytes andclimbers (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¡erentfern groups, speci¢c taxa, parents and allopoly-ploid o¡spring (see Section 3.11: Exploitation ofpotentials of polyploidy). They can also vary inrelation to location and habitat positioning withinthe same species (e.g. Cousens, 1981). Neverthe-less, in comparison with many angiosperms, over-all fern growth rates are relatively slow (least so insome epiphytes and some pioneer species), andthis has been suggested to be linked to the inher-ently slow rates of some physiological processes inferns (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 (Wongand Hew, 1976) and conductance of photosyn-thetic carbon assimilation in mainly C3 pterido-phytes, which are considered ‘‘generally towardsthe 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 Section2.1: The handicap of an independent gameto-phyte stage) also limit the capacity of pterido-phytes to adopt short life-cycle turnovers of thetype 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 cultivationwhere only a few exceptional examples havebeen met which display rapid life-cycle turnoversof the order of a year or less from spore-sowing tosporophyte ¢rst spore production. These occur ina few ‘modern’ genera (such as Anogramma andPityrogramma (both Gymnogrammaceae) andDoodia (Blechnaceae)) and represent under 0.2%of taxa personally cultivated in 40 years. Annualsare thus rare in pteridophytes as a whole, and thevery great majority of ferns are thus committedperennials, 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 thepast. Furthermore, there is also a general trendfor greatest longevity to be achieved amongst sev-eral taxonomically more ancient extant taxa (e.g.Osmunda, Angiopteris, Equisetum), which maymean that longevity may have been an even great-er feature of even more pteridophytes in the fossilrecord. That this is usually coupled to ultimatesize achieved should allow for appropriate fossilsignals to be identi¢ed and perhaps communityage-structure to be indicated, and might furtherindicate palaeo-sites of adequate habitat stability(see also Section 2.4: Intolerance of widely £uc-tuating conditions). Occurrence of multi-agedpopulations, including aged individuals, wouldimply 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 andPhillips, 2002-this issue).

2.4. Intolerance of widely £uctuating conditions

Intolerance by unadapted sporophytes ofwidely £uctuating conditions is a particularlyunder-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 theseat the levels at which these environmental in£uen-ces are met on initial frond expansion. Shouldconditions subsequently change (such as increasein light levels due to a tree fall gap forming in thecanopy) existing fronds appear unable to re-adapt. Only subsequently emerging fronds adaptas far as they are functionally able to the newconditions encountered. Plants may require afull growing season before all fronds borne be-come modi¢ed to any major features of environ-mental change. Furthermore, lack of stomatalcontrol, should conditions change, has been docu-mented in Lycopodium species, with modestamounts of inter-speci¢c variation (Heiser et al.,1996).Established sporophytes thus do not respond

well to environmental £uctuations, unless theyare ones to which a species is especially pre-adapted. It is probably such inherent incapabil-ities of short-term response that ensures thatfern sporophyte success is always greatest whenenvironmental 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 thetree canopy itself has mostly completed growth(Page, 1988). Little would be achieved, and thereis everything to loose, by timing frond-expansionto be any earlier than this. In tropical moist cli-mates, however, where there is year-round forestcanopy shade-provision, new fern frond growthcan occur throughout the year. By contrast tothe single spring growth ‘£ush’ of fern frondemergence of temperate regions, tropical fernfronds arise typically in a steady and sequencedyear-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 allsites, further micro-habitat variations appear tobe 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 subsequentdevelopment patterns of the plant. Such patternsmay 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, thenpalaeo-environmental conditions can be inferredfrom fossil fern £oras. For example, fern crownswith fronds and frond buds simultaneously atmultiple stages of development (either on individ-ual specimens or within populations) would beusefully 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 thesame stage would indicate growing-season releasewithin a more seasonally £uctuating environment.A further signal reinforcing the latter, but in thenon-growing season, might be the additional pres-ence of seasonally developed subterranean storageorgans. Root tubers on some ferns (e.g. Adian-tum), if fossilised, would indicate dislodgementduring a dry-season interval. Equisetum, whereclearly fossilised with tubers, would indicate fos-silisation in winter (between September and earlyApril in the northern hemisphere), and that theaerial parts would have been deciduous and thusnot simultaneously present.

2.5. Poorly controlled evaporative potential

The general need for moist environments, withlow evaporative potentials to counter high ratesof water loss, characterises much of the life-cycleof the majority of ferns (e.g. Wylie, 1948). Thisproblem places often severe limitations on the de-gree of exposure which can be tolerated by manyferns. Such poor control clearly restricts pterido-phyte and especially fern success on both a re-gional and a habitat basis, and is certainly alsohighly taxon-speci¢c. It is a noteworthy aspect ofthis limitation in living fern taxa, that individualspecies are often limited by particular levels ofsoil-water availability, as well as surrounding airhumidity. Furthermore, even within the samehabitat, di¡erent species can have subtly di¡eringrequirements, including lateral movement andparticular aeration levels of the soil water present.

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

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 justoverall 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 theseaspects even for living pteridophytes. It requiresdiligent e¡orts to draw such information togethereven for well documented areas such as Britainand Ireland (see, for example, maps of severalfactors 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 thepast, using approaches being more widely devel-oped (and funded!) mainly by agro-meteorologi-cal and forestry sources (see especially Thompsonet al., 2000). Fern £oras and nearest living rela-tives (‘indicator species’) could both be applied inpalaeo-environmental studies. Environmental in-dicators could be used, for example, for establish-ing relative comparisons between habitats andniches in separated palaeo-locations (cf. the mod-ern Equisetum example cited above).

2.6. Uncontrolled high reproductive commitment

Nearly all pteridophyte sporophytes, includingferns 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 aretypically produced in prodigious numbersthroughout the remaining life of the plant. Thismay 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 regularlyoccur in terms of what is necessary to maintainindividual 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 suchover production, and the inability of most ferns tocontrol it, must be a considerable drain on recur-rent energy commitments by the parent sporo-phyte. These levels of commitment, the apparentlyhighly sacri¢cial nature of much of the process,and the fortuitous roles of chance are probablylittle di¡erent in character today from those whichtypi¢ed the life histories of ferns through theirlong palaeo-history.This disadvantage is, however, a two-edged

sword, since some clear advantages may well alsobe gained by large spore numbers. These are dis-cussed in Section 3.5: High migrational ability ofthe airborne spore. Of these, signi¢cant in a pa-laeo-perspective are likely to be combinations ofrecurrent arrival at sites of poor access, abilities ofpotentially long-distance dispersal, and of rapidexploitation of sites immediately following post-disaster scenarios. All, and especially the latter,open opportunities for serial successions to beginto involve pteridophyte sporophytes from the ear-liest stages, in potentially large numbers. Thesehave, through the fossil record, doubtless greatlyin£uenced the overall ability of pteridophytes(and especially ferns) to become exploiters of theepiphytic niche. However, this may seldom be ahabitat of high preservation potential (Poole andPage, 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 ifonly as a ¢lm, is essential for sexual fertilisationby free-swimming motile antherozoids within theimmediate habitat niche in which the prothalli ofthe gametophyte generation actually grow. Apartfrom 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 whensuch free water exists. Observations in experimen-tal culture (Page and Walker, independent person-al observations) show that for some species thismay be as ¢nely tuned as speci¢cally timed an-therozoid release (and perhaps archegonial recep-tivity) over only certain periods in seasonal andeven diurnal cycles, with which such free waterhas to necessarily coincide. This is a little-appre-ciated factor which may well contribute substan-tially to detailed delimitation of pteridophyteniches, habitats and overall ranges, as well as hy-brid occurrence (and thereby evolutionary success(see Section 3.11: Exploitation of potentials ofpolyploidy).In this respect, the Pteridophyta as a whole are

very much the plant Kingdom’s equivalent of theAmphibia, between which there are many broadsimilarities 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 limitationsmust have applied at least equally stronglythroughout the pteridophyte fossil record, whereother pteridophyteâmphibian analogues mightalso exist.Clearly, for almost all pteridophytes, the achilles

heel of a free-water requirement will have beenexperienced throughout their past history, to thedegree that fossil pteridophyte presence is neces-sarily indicative of the presence usually moist en-vironments, in which adequate free-water (chie£yby precipitation) will at some time have beenpresent. To a large extent, pteridophyte taxonom-ic and morphological diversity today is a measureof the regularity and reliability of occurrence ofsuch water ^ ¢de the overwhelming abundancewhich ferns can achieve in the regularly moistcloud zones of tropical mountain mist forests to-day. (This limitation clearly links closely to thatof Section 2.4: Intolerance of widely £uctuatingconditions, and Section 2.5: Poorly controlledevaporative potential, and also to Section 3.3:High disease resistance under saturated humiditylevels). Sites of exceptional fern diversity withinthe fossil record, coupled with analysis of the eda-phic niches occupied by the species and life-formsinvolved, can potentially provide a valuable tool

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towards determining aspects of water availabilityin various palaeo-environments.

3. The recurring advantaging strategies of fernecology, adaptation and survival

In contrast to the seven limitations above, theadvantaging strategies of fern ecology (12 areidenti¢ed here as 3.1^3.12) are the ‘positive’ sideof fern potentials, adaptation and survival. Thesecompliment those of the ecological approach ofGrime (1977, 1985). These strategies re£ect recur-ring pteridophyte strengths today and are likely tohave done the same throughout the history ofpteridophytes.In deriving an analysis of these strategies, the

extant ferns provide a resource-rich informationbase, in which laboratory work and experimentalcultivation each contribute a substantial experi-mental database. The evidence is combined herewith information from the ¢eld to achieve anoverall broad ecological synthesis. The evidencesupports the view that many clear and de¢nableprinciples of survival exist amongst extant ferntaxa, governed by innate abilities of the plantsthemselves, and which occur across broad taxo-nomic spectra.

3.1. Low-light photosynthetic ability

Virtually all observational fern ecology todaywould support the view that many ferns surviveparticularly well in levels of light which are toolow for most competing angiosperms (as well asmany conifers) to tolerate, but I am aware of fewexacting physiological measurements which ad-equately quantify this. Complete photosyntheticsaturation at low levels of incident light wouldappear to be the key factor (Page, 1979b). Arina-wati et al. (1996), for example, quote high totalchlorophyll levels and particularly low light-satu-ration photosynthetic rates of fronds of the trop-ical climber Teratophyllum rotundifoliatum (whichhas fronds in both low and high light levels), andindicate that di¡ering in£uences of light type mayalso be involved.Fern species of low-light habitats (which are

very many, e.g. Plate II, 3) exploit a niche inwhich competition pressure today is substantiallyreduced. These abilities undoubtedly greatly facil-itate the occupation of a wide range of niches inforests, from deep shaded ravines to dark forest£oors, as trunk epiphytes and climbers, and asplants of highly cloudy or frequently misty envi-ronments. Low light-saturation e⁄ciencies willhave been a particularly important factor throughthe course of angiosperm radiation (e.g. Crane,1987). Such shade-tolerating potentials have al-most certainly been available to ferns in habitatsof earlier forest types too (e.g. Thomas, 1985) andcould 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) areknown in some palaeo-£oras (e.g. Rothwell etal., 1994; Stockey et al., 1999). Large and delicatefern fronds are also represented in the fossil rec-ord (e.g. Deng, 2002-this issue) and so are ferns ofthe shaded woody habitats of peat-formingswamps (Collinson, 2002-this issue; DiMicheleand Phillips, 2002-this issue; Van Konijnenberg-van Cittert, 2002-this issue). However, ferns ofshade 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) wouldseem to o¡er a particularly low potential to nor-mally become well-represented (at least as macro-fossils) in most fossil £oras. By contrast, thecoarser-textured often higher biomass, toughstructures (especially stipes) and frequently moremonospeci¢c counterparts (e.g. Plate I) of moreopen habitats have higher fossilisation potential(e.g. Collinson and Ribbins, 1977; Yao and Tay-lor, 1988; Skog, 1992; Rees, 1993; Gandolfo etal., 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 accountwhen interpreting fern £oras of the past.

3.2. Diverse phytochemical armament

Mostly only becoming known in the last 25 yr,

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diverse phytochemical armament is probably themost e¡ective and widespread strategy in promot-ing direct vegetative survival of Pteridophyta as awhole. It is becoming clear that phytochemicalarmament, of widely di¡ering degrees and types,is taxonomically widespread in ferns and otherpteridophytes, 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 slowgrowth rates (see Section 2.3: Slow plant growthrates), vulnerable growing points and organs andlack of most other physical defences or herbivoreavoidance mechanisms (see Section 2.2: Singlegrowing-point limitations of sporophyte architec-ture). It probably also contributes substantially tothe survival of gametophytes, and thus to mitigat-ing against the apparent vulnerability of this free-living stage (see Section 2.1: The handicap of anindependent gametophyte stage). Such biochemi-cal armament, however, undoubtedly requirescontinuing resource and energy commitments onthe part of the plant, but it avoids the need fordevelopment of elaborate physical defence struc-tures, thus enabling relatively simple pteridophytearchitectural form to persist.Nevertheless, remarkably little is yet under-

stood about which of any known phytochemicalsubstances are employed to achieve e¡ective de-fence and exactly what they are targeted against.Currently we are only aware that present targetsseem broad, and were probably similarly so in thepast. Field botanists will be aware, however, thatfew modern ferns usually show signs of any sig-ni¢cant herbivory in the ¢eld. Even to a humannose, many ferns have distinctive (and often spe-cies-speci¢c) odours (e.g. Plate II, 2), some ofwhich are quite curious: e.g. the temperate Gym-nocarpium robertianum (Athyriaceae) which hasan apple-like fragrance, Polypodium glycyrrhiza(Polypodiaceae) which smells of liquorice, andthe tropical Anemia phyllitidis (Schizaeceae) whichsmells to me of running model railways!). Theresearch which is available suggests that, in mostferns, 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; Balick et 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 anyother fern, and provide a valuable generic exam-ple. Pteridium is known to contain a particularlyformidable armoury of repellents, from tanninsand sesquiterpenoids to phenols and cyanide (asa cyanogenic glycoside), plus two carcinogens, aleukaemiagen and, for good measure, a broad-spectrum insect ecdysone. Collectively, or sepa-rately, these can have dire e¡ects on potentiallybrowsing 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¢eldand 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 copiouslyproduced by bracken (e.g. Gliessman, 1976;Gliessman and Muller, 1972) and probably bymany (? most) ferns (Weinberg and Voeller,1969; Banerjee and Sen, 1980). Furthermore, atleast in Pteridium, the spores also are known to besubstantially armed with some of the same com-pounds in even higher concentration per dryweight than in the vegetative body of the plant(Evans and Galpin, 1990). These compounds arepresumably e¡ective against sporophagy duringboth pre-dispersal and post-dispersal phases.Fern fronds can and do, however, provide

roosting-habitats for a great number of terrestrialarthropods (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 successfullyco-exist. A limited tolerance to a degree of grazingappears to exist between ferns and some insects,notably Lepidoptera and sometimes Hemiptera(Balick et al., 1978; Lawton, 1982; Lawton andMacGarvin, 1985; Weintraub et al., 1995). Addi-

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tionally, various ant^fern associations and mutu-alisms are becoming recognised (e.g. Darwin,1877; Southwood, 1977; Page, 1982a; Lawtonand Heads, 1984; A.F. Tryon, 1985; Walker,1985; Arens and Smith, 1998). Sometimes furtherdefensive bene¢ts to the plant may be gained bytolerating the presence of such animals, and somedefence 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 andyoung sporophytes which are especially attractiveto rapid and usually terminal depredation bysmall slugs. However, in the wild, this species isregularly and aggressively ant-colonised (and ishere inferred to be likely to be mutualisticallyant-protected) on the branches of the tropicallowland swamp-margin trees on which these largeepiphytes normally grow (Jermy and Walker,1975). It is presumed here that chemical defenceshave been dropped when other alternative (lessenergy-consuming) defence mechanisms have be-come available. Our observations showed that thesame slugs and snails did not similarly attack abroad range of other adjacent fern cultures. Thisprovides at least some negative evidence of a nor-mal defence in most pteridphytes (presumablychemically mediated) which would appear to besensed, 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 againstbrowsing pressures, especially by arthropods (e.g.Wootton, 1981, 1990; Scott et al., 1985, 1992,1996) that selection pressures for the developmentof such a diverse array of phytochemical arma-ment (and a diversity of arthropod counter-mea-sures) will have been recurrently stimulated. Veryfew other ferns have been studied in any compa-rable detail to Pteridium, although the list of taxaand known phytochemical isolates and their di-versity of e¡ects on modern browsing animalgroups is steadily growing. The extent of these

indicates a high probability that such defencesare general in most living pteridophytes. Theycan be varied (e.g. through a number of di¡erentsecondary 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 degenerativeconditions in a broad spectrum of animals expe-riencing them. Other contained compounds, suchas ecdysones, are more arthropod-speci¢c.Also essentially phytochemical in origin (and

almost worthy of a separate entry as a furtherindependent advantaging attribute of ferns, werethere clearer evidence), is the occurrence in fernsof chemically unusual intra-cellular cements,which bind cells together (Manton, 1950). As faras I am aware, in contrast to all phytochemicallytoxic aspects of ferns, nothing is known aboutthese, beyond that they contrast with those ofall £owering plants. In ferns, these have the reputeof not being soluble in hydrochloric acid, and ofhence making fern frond material indigestible toall animals dependent on an HCl-mediated diges-tive system. Indeed, slugs and snails are the onlyanimals known (at least by repute amongst pter-idologists) to have the necessary stomach enzymeswith which to attack these fern cements. I person-ally regard this as a potentially important survivalstrategy in ferns (and possibly in other pterido-phytes) against animal depredation, but, so faras I am aware, the whole topic appears virtuallyunresearched. It could, however, have consider-able implications both for the survival of fernsagainst a range of herbivores through time. Fur-thermore (especially if it also operated against de-cay organisms ^ I do not have any evidence eitherway), it may also have a¡ected the preservationpotential 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 Oribatidmites ^ 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

PALBO 2428 5-6-02


fern leaves were already then less browsed thanalternative vegetation (e.g. Beck and Labandeira,1998; Collinson, 1996, p. 380^381) and, althoughthe Palaeozoic tree fern Psaronius exhibits a hostof arthropod interactions these do not seem toinclude leaf-feeding (Labandeira, 2001). Duringthis long period of interaction, evolutionary pres-sures for the development of adequate armamentmust have been intense, constant and diverse inmost habitats in which Pteridophyta have suc-ceeded. Clearly modern ferns enjoy considerableabilities to achieve complex biochemical defencepotentials (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). Doubtlessmany other variations have occurred through thefossil record against the same selection pressures.Increasingly, evidence is that the pathways ofknown defence involved are, chemically speaking,complex; biologically speaking, e¡ective; andevolutionarily speaking, diverse and often subtle.The main measure of the speci¢c e⁄cacy of bio-chemical defences through the fossil record ismost likely to be gained through assessments ofactual recordable incidences (and hence inferredsusceptibility) of browsing activity (foliar/spore)between contemporaneous taxa and throughtime (like that of Wilf and Labandeira (1999)for angiosperms). Unfortunately, for the fossilrecord, those taxa which were highly susceptiblewill be those least likely to be represented. How-ever, clearly the Pteridophyta are not mere begin-ners at these diverse and extensively practisedachievements!

3.3. High disease resistance under saturatedhumidity 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) andachievement of successful germination and estab-lishment (see Weinberg and Voeller, 1969; Dyer,1979; Lloyd and Klekowski, 1970; She⁄eld, 1996for reviews), ferns succeed under humidity re-

gimes within which most £owering plant seedlingswould readily ‘damp-o¡’ through rapid fungal at-tack. Cultivation experience shows that intrinsicpathogen 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 ecologicaladvantage of the fern. Extreme examples mustbe the ¢lmy ferns (Hymenophyllaceae), many ofwhose 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 inferns (e.g. Kobayashi et al., 1975; Banerjee andSen, 1980).Thin-fronded ‘¢lmy ferns’ (which have been as-

signed to the Hymenophyllaceae) are known fromthe Mesozoic (Deng, 1997; Axsmith et al., 2000)implying a long history for ferns growing in satu-rated humidity levels. Signi¢cantly, many of theferns in a diversity of distantly related families inthis habitat today are successfully bulbiferous,often developing a ‘walking-fern’ habit and/or de-velop axillary branching patterns of growth. Suchhabits occur in few other habitats, and hencewould provide an important marker in the fossilrecord for such humidity and moisture regimes.

3.4. High tolerance of acute nutrient disequilibriumsubstrates

Two suites of factors here (which could almostrank as separate advantaging strategies in theirown right) operate either independently or collec-tively in achieving unusually high and varied nu-trient disequilibrium tolerance amongst modernferns.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 tolerateadditional unusual levels of excess mineral ele-ments which can also be present in some of theseterrains, and which can be at levels that would betoxic to many other plants (e.g. Plate II, 6).Field ecology suggests that these tolerances ap-

PALBO 2428 5-6-02


pear to be possessed, either separately or collec-tively, within an especially wide taxonomic arrayof 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 ofactual 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 onthis. Amongst the ¢rst suite, subtle di¡erencesamongst tolerances of epiphytic taxa are re£ectedin the tendency (in the tropics especially) for dif-ferent pteridophyte epiphytes either to be general-ist or more narrowly specialist species as far aspreferred 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 evolvedvery numerous times in ferns, adapting individualtaxa closely and subtlety to e¡ective exploitationof particular local habitat opportunities.There are strong contrasts between the ability

to succeed in the ¢eld on generalised, open, butstrongly limited terrains versus (at the extremeopposite) within exuberant mature mesic forestvegetation. These contrasts emphasise the rolesof physical/chemical versus biotic pressures withwhich respective pteridophytes are confronted.Mature forest vegetation, and especially rain-

forest, is widely appreciated to be a very complexcommunity, 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; Poulsenand Neilsen, 1995; Poulsen and Tuomisto, 1996;Tuomisto and Poulsen, 1996). Most pteridophytespecies from such sources can be successfullyreared in glasshouse culture (personal observa-tions 1958^2001) on relatively arbitrary standard-

ised horticultural compost media (including,ironically, most epiphytes, providing that theyare not over-fed with standard nutrient additives).This indicates that the often high localisation offorest species in the ¢eld is not purely (or evenmainly) the result of narrow mineral tolerancesand speci¢cities (beyond the general one of epi-phytes). Instead, the niche-width of these in thewild (often extremely narrow, sometimes alsohighly 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 virtuallyzero) biotic competition can open wide habitatopportunity for those species which are able toachieve high tolerance levels of the ruling nutrientdisequilibriums. For these, the edaphic speci¢citycan seem very high. Yet many pteridophyteswhich are vigorous (sometimes to the extent ofbeing 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, Matoniaand Christensenia, and most Schizaeaceae) can,ironically, prove extraordinarily di⁄cult to growat all in conditions of experimental cultivation!Extremely high and exacting directly edaphicallylimited tolerances and limitations seem indicatedfor such pteridophytes.Both suites of this nutrient disequilibrium tol-

erance strategy, either separately or in combina-tion, advantage ferns in enabling them to grow ina 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 ofthese abilities is to open a variety of low-competi-tion habitat opportunities for colonisation intosites which can be widely available to pterido-phytes because of the migratory e⁄ciency of theairborne spore (see Section 3.5: High migrationalability of the airborne spore). Typical habitat ex-amples include:

b intrinsically nutrient poor sandy heathlandsand savannahs;

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

PALBO 2428 5-6-02


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

b newly formed volcanic ash surfaces;b post-wild¢re sites;b erosion surfaces of lithophytic sites ;b habitats of high metalliferous availability

such as ultrama¢c soils and man-made metallifer-ous mine spoils ;

b epiphytic habitats.Wide arrays of fern species from diverse fami-

lies are today specialist colonists of many of thesesites, with considerable specialisations especiallyof 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 ofthe low-nutrition suite, and subtle levels of bioticcompetition are probably also involved in di¡er-entiating between di¡erent ‘preferred’ epiphyticsubstrates. Despite these limitations, an enormousnumber of pteridophyte (especially fern) epiphytespecies exist. Some (e.g. species of Tmesipteris) arethemselves specialists mainly of tree-fern trunks,even to genus (Dicksonia), while the majority evenspecialise in the occupation of speci¢c branchniche locations (often prescribed by their mor-phology) and tree canopy heights occupied onparticular tree species hosts. The whole epiphyticpteridophyte suite is composed of an enormousrange 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 onwhich 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 amaximum is limited to that of the tree on whichthey grow. Many fall in storms, often driven bytheir own weight, where they die and decomposerapidly on the forest £oor, due to combinations ofconstruction of many soft and semi-succulentparts as a consequence of their growth rates.By contrast, ultrama¢c sites clearly require un-

usual degrees of tolerance levels from both suites,and the levels of such tolerances often appear tobe highly taxon-speci¢c. A smaller diversity ofplant habits is present, with plants usually ofsmall size, scattered (seldom contiguous) occur-rence, and tough, leathery growth. Dead fronds,frond debris and especially frond bases may per-sist around parent plants for years. On directlynutrient poor edaphic sites, either characterisedby post-¢reburn environments or (especially) byerosion-regimes and constant surface moisturedownwash such as today on high-mountain sad-dles, notably sprawling and often rampant pteri-dophyte habits are especially characteristic, withtough growth structure typically yielding muchlocal 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 relatedtaxa and their adaptations, suggests a long pasthistory for this phenomenon. Sites of unusualmineral availability must have always occurred,while ¢reburn sites, some with ferns, are knownsince at least the Early Carboniferous (¢de Scottand Jones, 1994; Falcon-Lang, 1998, 1999; DiMi-chele and Phillips, 2002-this issue). Volcanic ashhabitats, also with ferns, are known from at leastsimilar times (Scott and Galtier, 1985; Brous-miche et al., 1992; Crowley et al., 1994). Theantiquity of this strategy, which probably enabledopportunistic colonisation even among early ¢li-caleans, is further indicated by Galtier and Phil-lips (1996). Epiphytism amongst ferns, althoughvery fragmentarily known (e.g. Sahni, 1931;Rothwell, 1991; Poole and Page, 2000) has avery 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 taxaby the occurrence of taxonomically outlying andpresumed relictual species of ferns associated withapparently relictual conifers as enclaves on someheavily 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 abilityto colonise a variety of low nutrient habitats is

PALBO 2428 5-6-02


a strategy which is probably widespread throughthe fossil record for Pteridophyta, and doubtlesshas included, within its exponents, many di¡erentgroups of ferns. Many terrestrial ferns as far backas the Early Carboniferous have ‘sprawling’ or‘rampant’ habits (DiMichele and Phillips, 2002-this issue) and one cannot help but note thatthis habit is characteristic of extant pteridophytessurviving 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 advantagesarising 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 threeare clearly available. Furthermore, all are notonce-only events, but apply continuously to sporegeneration and release processes in most ferncommunities.All spore dispersal achievements are described

here as ‘potential’ since to what degree they areactually realised in nature is clearly complex andis yet only fragmentarily understood. Many var-iations in circumstances must apply. Exactly howsigni¢cant long-distance dispersal might be inpteridophytes has, for example, long been a topicof debate (e.g. Gregory, 1945; Lloyd, 1974a,b;Parris, 1985; R.M. Tryon, 1985, 1986; Kendallet al., 1986; Lacey and McCartney, 1994; Caul-ton et al., 1995; Schneller, 1996b), though thereare few exacting data on this issue.My own interpretations are based on three lines

of evidence: (1) my personal ¢eld experience offern £oras on oceanic islands in three majoroceans today; (2) the known longevity of widetaxonomic arrays of fern spores in captive storage

(4^25 yr in packets, a maximum of 63 yr recordedon an herbarium sheet) ; and (3) the known resis-tance of fern spores to environmental hazards (seePage, 1979b for an earlier review). These interpre-tations, however, equate closely with those de-rived by Cousens (e.g. Cousens et al., 1985, andpersonal communications 1980^1986), also basedon independent experimental studies and parallel¢eld observations, which included the appearanceof taxonomically novel pteridophytes along theAmerican Gulf Coast following episodes of hurri-cane damage. I take a pragmatic approach andsimply begin from the practical stand-point thatall 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 sporedensity dilution away from the parent plant.However, spores can also disperse in long andsteady smoke-like plumes, and once airborne,can enjoy great resistance to known environmen-tal hazards (see Section 3.6: Spore tolerance ofadverse aerial environments). I conclude that itis not dispersal per se that is usually limiting interms of achievement of dispersal potentials inpteridophytes (and that endless discussion offern-spore migration abilities is a red-herring interms of dispersal usually achieved). Instead, itis the opportunities for establishment of arrivingspores, against indigenous biotic competition, thatis the real issue determining and confronting eco-logical achievement and ultimate range: create theappropriate habitat, and the appropriate pterido-phyte coloniser will, sooner or later, appear there.The likely e¡ect of distance is usually to in£uencethe timing, rather than the actuality, of the event.In this, disturbance regimes especially promoterenewed colonisation opportunities, almost irre-spective of where located, and biologically it isprobably those few spores that actually do getfar that are the real ecological and evolutionaryachievers.Some genetic evidence, which appears to sup-

port these views, has been recently gained in thecase of the rare fern Dryopteris remota (Schnelleret al., 1998). Furthermore, the activeness of manypteridophyte discharge mechanisms would appearto have evolved particularly in response to selec-tion pressures to optimise high mobility gain,

PALBO 2428 5-6-02


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-distancedispersal must self fertilise if it is to establish a¢rst colonising sporophyte. Most ferns appear tohave this potential (see Section 3.7: Flexibility ofbreeding systems to match varying ecological op-portunity). A genetic consequence of this is, ofcourse, that restoration of the diploid chromo-some number ensures that every gene becomeshomozygous and thus phenotypically expressedin the new sporophyte, irrespective of whetherthat 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¡erentin detailed adaptation to those of their previouspopulation, and on which natural selection forthat location at that time can consequently oper-ate. This would seem to be particularly signi¢cantboth today and through geological time in theevolution of the fern £oras of remote sites, andespecially 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 havebeen so virtually throughout the history of landplants. In combination with some of the abovetolerances, perhaps the most spectacular palaeo-examples of the ‘spore-rain’ potential have beenrapid achievement of ‘fern-spikes’ following thegreat environmental disturbance events of theCretaceous^Tertiary and perhaps also the Trias-sic^Jurassic boundaries (e.g. Spicer, 1989; Fowelland Olsen, 1993; Srivastava, 1994; and see alsoCollinson, 1996, 2002-this issue, for discussion).

3.6. Spore tolerance of adverse aerial environments

Virtually all of the potentials outlined abovewould be negated if the fern spore was not viableon arrival at a potential germination site. Longdistance dispersal may involve exposure to arange of aerial extremes en route, including thoseof extreme dryness, cold temperatures and irradi-ation. Much of the earlier data on this topic (see

Page, 1979b) still remains valid. This leads to theview that ferns spores are highly resistant to vir-tually all of the conditions which they might beexpected to meet during the course of airbornedispersal, even were this to be prolonged and athigh altitude.Additional aspects of spore viability-persistence

in the ¢eld in relation to soil spore banking havealso recently been discovered in ferns (Dyer andLindsay, 1992, 1996; Lindsay et al., 1994).Schneller (1996b) has further shown an importantcontribution by banked spores in helping toachieve a potential, when exhumed, of formingmany di¡erent genotypes at any location withinthe population’s area. Furthermore, there is greatdiversity in the architecture of fern spores (see, forexample, the many excellent illustrations of Tryonand Tryon, 1982), yet almost nothing is knownabout the adaptive and ecological signi¢cance oftheir varying morphological characteristics. Somediscussion of possible functional roles of sporeornamentation 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 proportionsof Pteridophyta in the £oras of oceanic islands(see Section 3.5: High migrational ability of theairborne spore), demonstrate the e⁄cacy of this,and may well have been one of the main selectionpressures for achievement of such viability poten-tials. Floristic patterns between such areas in thefossil 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 providea basis for future study of this topic.]

3.7. Flexibility of breeding systems to matchvarying ecological opportunity

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

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mating-system patterns are generally recognised inferns: sel¢ng (1) within or (2) between prothalli ofthe same parent sporophyte (intragametophyticand intergametophytic sel¢ng, respectively) and(3) outcrossing between prothalli arising fromthe 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 inhetersporous ferns, in the majority of living ferns(which are homosporous) mating-systems are to ahigh degree £exible and opportunistic. The pro-thalli of homosporous ferns have, in general, bothmale (antherdial) and female (archegonial) or-gans. There is normally a time-phase di¡erentia-tion between maturity of the organs of the twosexes. However, there may also be a period ofoverlap, and for most taxa, so far as is known,either intragametophytic and intergametophyticsel¢ng can be an option only if out-fertilisationby intergametophytic crossing fails. Outcrossingis thus likely to be e¡ectively realised whereverappropriate opportunity arises, and, with certainlimitations (Schneller, 1996a), most ferns arewidely regarded as being extreme outcrossers,with only a few nearly exclusively inbreedersknown (e.g. Ranker, 1992; Soltis and Soltis, 1992).Where whole populations of prothalli exist,

then sexual balances amongst prothalli growingfrom homosporous spores are known to be fur-ther mediated by antheridiogens (e.g. Schneller etal., 1990; Korpelainen, 1997), the in£uence ofwhich further encourages outcrossing and mini-mises sel¢ng. In wild prothallial populations, thee¡ects of such antheridiogens can be enhancementof the reproductive success of small gametophytesthrough promotion of gender expressions, whichwould not necessarily otherwise occur (Hamiltonand Lloyd, 1991). The e¡ects of antheridiogenscan operate between prothalli of di¡erent speciesin establishment of contrasting sexuality. This isprobably one of the factors promoting the num-ber of independent congeneric hybrids whichhave been ¢eld-recorded in pteridophytes (seeRothmaler, 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 forreviews).Thus, in addition to examples of ecological in-

£uences, we also need to look at breeding systems.These genetic potentials have probably becomeincreasingly varied and sophisticated through evo-lutionary time. Nevertheless, many must be an-cient in their basic origins and e¡ects, helping tounderpin a great diversity of fern ecologicalachievements throughout the fossil record. Aswith phytochemical armament (see above), thereis much work yet needed in drawing comparisonsbetween the breeding systems of more primitiveand more advanced living taxa and setting thisagainst the known fossil history and ecologies ofthe 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 andCheilanthes (Sinopteridaceae) (originating fromthe Canary Islands) which were tested on an ex-ploratory basis, showed exceptional abilities towithstand complete desiccation for enduring peri-ods. Such desiccated prothalli were successfullyrejuvenated from a ‘crisp and dry’ completelyair-dry state after storage for many months, byeventual return of overhead application of freewater, imitating rain.Not all cellular sectors of each individual pro-

thallus necessarily survived such treatment, butenough green tissue persisted in most to act as‘revival centres’ from which new growth resumed,and from which complete new prothalli with newsex organs then grew. Indeed, frequently morethan 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 ofa completely new ‘replacement’ generation ofsporophytes. 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 ofthis ability in ferns appears to have been littleappreciated and I am not aware of any otherstudies that have been made since. The lack ofextensive experiment across a broad taxonomicand habitat basis means that the extent of thisability 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 whichmay well have been of signi¢cance in the past.Prothalli could succeed under moisture regimeswhich are intermittent and unpredictable, on a‘try and try again’ basis after an initial prothallialfoothold has been successfully gained. Such pat-terns of survival could be advantageous in a num-ber of di¡erent habitats, varying from sub-desertsites to rock face habitats and even epiphyticones. In this behaviour, fern prothalli of a rangeof genera are displaying a similar, if unexpected,behaviour to mosses, suggesting that it could wellhave relevance for the processes of fern-colonisa-tion even in apparently hostile conditions, bothtoday and in the past.

3.9. Potential longevity of resultant sporophytes

An often overlooked advantaging strategy,sporophyte longevity, may well be a particularfeature of more ancient plants. It is also widelypresent in extant conifers (Page, 2002a,b), andhere too relatively especially so amongst manymore ancient members. In ferns, examples ofsporophyte longevity include tree ferns from 150to 200 years (e.g. in cultivation at Penjerrick Gar-den in Cornwall) and Osmunda plants said to beup to 300 years old in cultivation. In the wild, therhizomatous fern Platyzoma is estimated to beabout 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 perhapsthat, in contrast to species with rapid life-cycleturnovers, rates of adaptive change are committedto 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

potentials of polyploidy). Main achievements ofsporophyte longevity are:(1) capitalisation on success of achievement of

the gametophyte stage and subsequent physicalretention 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 ofyears: this is of particular advantage, for example,in achieving successful colonisation of habitatswhich appear only sporadically.Assessments of longevity in fossil pteridophytes

in relation to past selection pressures in di¡erentenvironments would be valuable. However, it isvery 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 havebeen similarly so. Therefore, amongst the giantCarboniferous representatives of these plantssporophyte longevity was probably the norm.

3.10. Exploitation of mycotrophy

Mycorrhizae have been widely recorded in as-sociation with the roots of extant ferns in ¢eldsurveys in widely scattered locations (e.g. Burge¡,1938; Cooper, 1976; Iqbal et al., 1981; Newmannand Reddell, 1987; Jones and She⁄eld, 1988;Gemma et al., 1992; Moteetee et al., 1996). Thissuggests that such associations may well be a nor-mal feature of the roots of the majority of extantferns 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 ¢eldgametophyte and sporophyte generations, is moreobligate 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 culturewhich indicate that gametophytes of virtually allleptosporangiate taxa tested will grow successfully

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aseptically, but there are other claims that ‘best’growth is achieved when prothalli have access tonormal soil fungi (e.g. Hutchinson and Fahm,1958). Where associations are facultative, it wouldseem most likely that these could most advantageferns either in terms of growth, perranation or inachieving exploitation of unusual and perhaps ex-acting ecological habitats, but remarkably little isknown about this. By complete contrast to ferns,I know of no reports of mycotrophy in horsetails,though experiments I have carried out growingroots of Equisetum in aqueous culture (Page,1967b) show that the sporophyte itself has longand unusually persistent root hairs, which maywell 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 plantssince at least the Early Devonian (e.g. Taylor,1990; Banks and Colthart, 1993). Data linkingbetween past pteridophyte diversity and exploita-tion of mycotrophy would be valuable, since suchrelationships 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 thepotentials of polyploidy (and especially allopoly-ploidy) has made to the achievement of speciationin ferns has been one of the main areas of newunderstanding 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; Werthet al., 1985; Soltis and Soltis, 1987; Barrington etal., 1989; Hau£er, 1989a,b, 1992; Wolf et al.,1990, 1991; Rabe and Hau£er, 1992; Hau£er etal., 1995). It has become clear that while autopo-lyploidy is only an occasionally successful evolu-tionary route in ferns, allopolyploidy is widelysuccessful (Walker, 1979, 1985; Hau£er, 1996).Allopolyploidy allows for existing genomes to

be recombined in new and fertile taxa. It providesa rapid route for species evolution and adaptationin ferns, and, where most successful, it tends to

produce plants of enhanced vigour, typically re-£ected in increased size and/or faster vegetativegrowth rates. Ferns have large numbers of smallchromosomes in cells with high cytoplasmic vol-ume ratios. This enables many stages of chromo-some doubling to be successively accommodatedupon one another, while maintaining full opera-tional integrity of the cells themselves during theircrucial mitotic and meiotic divisional processes.Allopolyploid-derived tetraploids, octoploids andploidy levels up to 16 ploid are known, and maybe higher than this in some genera whose basenumbers are uncertain. Back-cross hybridisations,between members of di¡erent ploidy levels withingenera, appear to be just as common as crossesbetween those of the same level. The permutationswhich can result are many, progressively buildingcomplex 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 recentlycon¢rmed by molecular work, for example in Po-lystichum ^ Mullenniex et al. (1998). In additionthere are multiple hybrids at the same ploidy lev-el, some of which produce a percentage of appar-ently good spores (Page, 1963, 1990a, 1997b). Amechanism for stabilisation of hybrid reproduc-tion at a homoploid level, autogamous allohomo-ploidy, has also been proposed (Conant andCooper-Driver, 1980). Opportunity also existsfor changes in mating systems, high genetic heter-ozygosity, the survival of genetic redundancy andthe ability for species, including narrow endemics,to store high genetic variability (e.g. Chapman etal., 1979; Gastony and Gottlieb, 1982). Also aninitially limited gene pool of an allopolyploid maybe 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 etal., 1987, 1990). The whole process results in thecreation of morphological and ecological novelty,

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genetic diversity, maintenance of fertility, andclear separation of genetic identity between dip-loid progenitors and polyploid derivatives. Thepractical 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 thanthe 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 mayarise, will be seldom necessarily more successfulthan their parents if these are already ecologicallywell-adapted. However, in more actively evolving£oras and under more changing environments,higher ploidy derivatives can more often ¢ndniches clear for ecological success, probably even-tually displacing many of the original ancestraldiploids. An extreme range of contrasts amongstfern ploidy spectra is thus apparent. The long-sta-ble and highly encapsulated fern £ora of the Can-ary Islands has well under 30% polyploidy andthese only of low ploidy grades (Page, 1967b,1973). This can be compared with the less con-¢ned and more actively evolving fern £oras ofeither post-Pleistocene deglaciated areas of Eu-rope (e.g. Manton, 1950; Vogel et al., 1998). orwith what have been widely regarded as moremodern 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, ismore typical. The former circumstances thushave the greatest possibility of preserving relictualtaxa in ferns (with many of the ferns of the Can-ary Islands, for example, surviving today littlechanged since the Miocene ^ Page, 1967b), thelatter for the success of much newer diversity.Even if only some of these aspects have applied

throughout the past history of ferns the potentialconferred on ferns to meet new environmentalchallenges is clearly high. These mechanismsmay well have contributed signi¢cantly and sub-stantially to fern ecological adaptive change andhence long-term fern survival and diversi¢cation.Evolutionary stasis, perhaps in part involving

ploidy stability and in part related to life-cyclelongevity, has been identi¢ed in several generaand 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 ofpast activity in some ancient lineages, such asOphioglossum and Equisetum, while mechanismsare also provided whereby opportunities for newdevelopments from old stocks (e.g. Page andBarker, 1985; Ollgaard, 1992) can also rapidlyoccur.

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 gainadditional protection of their whole vegetativestructure by attracting ants (see Section 3.2: Di-verse phytochemical armament), there are fewother pteridophyteânimal associations. The onlyones of which I am aware, are the spiny spores insome Isoetes species (e.g. I. echinospora) whichappear to be an adaptation to bird dispersal(Page, 1982b). Also some echinate spores, andthe unusual lasoo-like ¢lamentous outgrowths ofspore walls in Lecanopteris mirabilis, have beensuggested to be an adaptation to spore transportby the sporophyte’s associated ants (A.F. Tryon,1985, 1986). It is, however, noteworthy that onlya very few known examples exist and a certainlevel of quite local evolutionary experiment seemsindicated, with methodologies which, in pterido-phytes generally, appear not to have becomewidespread.Throughout the vast bulk of pteridophyte di-

versity, there appears to be remarkably little de-pendence on animals in general achievement ofthe main life-cycle functions of vegetative growth,propagule dispersal or sexual achievement. Mostferns consequently constantly ‘shun’ rather than‘court’ most animal species. This is in great con-trast especially to the £owering plants, wherecourting of animals (especially of pollinating in-

PALBO 2428 5-6-02


sects by £owers) has enabled often complex andsometimes bizarre pathways of achievement toevolve which are presumably more e¡ective thancould be achieved without such support.Two important advantages accrue, however, for

ferns:(1) Having established e¡ective pathways of

biochemical defence mechanisms (see Section3.2: Diverse phytochemical armament), there isan uncomplicating freedom to apply these withoutlimitation throughout all the varied stages of theplant life cycle.(2) It has enabled the main life processes of

Pteridophyta, including dispersal and mating, tobe achieved virtually exclusively with the presenceof 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. Thishas contributed enormously to the fern’s freedomof specialisation in defence through the develop-ment of whole cocktails of diverse chemicalagents, against which animal groups are leastlikely to evolve complete defences. For example,in combination with other agents, the productionof insect ecdysones by ferns must be a defence towhich 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 probablybegan with the ¢rst vascular land colonisers.Thereafter, through the dependence for dispersaland reproduction solely on only uncomplicatedphysical 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 whatthese plants have been able to achieve, and con-sequently to the close comparability betweenmodern 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 speciesof ferns alone. In terms of species richness, homo-sporous pteridophytes are more successful than allother non-angiosperm grades combined (Roth-well, 1996a). This account demonstrates that,amongst pteridophytes, similar general responsesare 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) offerns and fern allies today, an attempt is madeto analyse why pteridophytes are able to colonisesuch a range of habitats, and especially so manymarginal ones. This synthesis is used to derivebasic principles concerning the innate biologicalweaknesses (limitations) and special strengths (ad-vantages) of Pteridophyta as a whole, which arepresented here.The seven limitations identi¢ed are innate

weaknesses of pteridophytes, which clearly limitfern potentials and achievements today. Clearly,none of these have been able to be successfully‘thrown-o¡’, to any major degree, in the courseof pteridophyte evolution. On this evidence, allmust have acted as similar limitations throughoutpteridophyte evolutionary history. Interestingly,few of these (perhaps only the single growingpoint (Section 2.2: Single growing-point limita-tions of sporophyte architecture)) might be de-duced directly from the fossil record itself, andmost would therefore be unknown if we did nothave evidence from the living plants.By direct contrast, the 12 advantages conserva-

tively identi¢ed (14 if including subcategorieswithin Section 3.2: Diverse phytochemical arma-ment, and Section 3.4: High tolerance of acutenutrient disequilibrium substrates) clearly openopportunity 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 indicatesthat most of these advantages appear broadly

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across most taxonomic groups and seem to havedeep-rooted origins within Pteridophyta, to thedegree that many are judged to be special innateabilities of these plants. On this evidence too,most must have also been available to operatethroughout pteridophyte evolutionary history.Some, such as tolerance of extremes of edaphicconditions, may have actually directly helped sur-vival of several ancient fern genera to occur(Page, 2002d). Interestingly again, a few mightbe proven, some others inferred, but many wouldalso remain unknown, especially in the potentialswhich they liberate, if we did not have evidencefrom 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 waterto breed’ are all to a degree o¡set by the abilitiesconferred by high disease resistance under satu-rated humidity levels. Upon this balance, low-light photosynthetic abilities then enable manysuch high-humidity but necessarily low-illumina-tion habitats, in which biotic competition levelsare generally low, to become exploited to thefull. Slow plant growth rates may be less of ahandicap 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 othermarginal 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 arepartly o¡set by many speci¢c morphologicaladaptations 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 fernsfor sites of acute nutrient disequilibrium as wellas the access to these regularly gained by the highmobility of the airborne spore. Animal browsing

is also targeted by the diverse phytochemical ar-mament of pteridophytes, which has a broadspectrum of e¡ects on animals, especially againstinvertebrates. Uncontrolled high reproductivecommitment, although doubtless a highly en-ergy-intensive process, is combined with potentiallongevity of resultant sporophytes. Together theseattributes 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 areclearly consequent on dispersal opportunities, no-tably the facultative inbreeding fallback whenoutbreeding 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 extensiveexploitation of potentials of polyploidy (especiallyallopolyploid progression) and their high degreeof biotic independence. It is inferred that theseare also attributes with a long past history.Amongst living pteridophytes, ancient elements

as well as modern elements often co-exist (Stewartand Rothwell, 1993). Many fern families, notablyMarattiaceae, Osmundaceae, Schizaeaceae, Glei-cheniaceae, Matoniaceae, Dipteridaceae, Dick-soniaceae, Cyatheaceae, Azollaceae, Salviniaceaeand Marsileaceae, have well established, extensivefossil records (Collinson, 1992, 1996, 2002-this is-sue; DiMichele and Phillips, 2002-this issue; VanKonijnenberg-van Cittert, 2002-this issue). Othernon-fern pteridophytes, especially Equisetaceae(Page, 1972a,b), Selaginellaceae (Page, 1989) andLycopodiaceae (Wikstro«m et al., 1999) show evi-dence of adaptive traits which must also have oc-curred in the past biology, ecology and ancientmorphologies of these groups. Periods of evolu-tionary stasis have been recognised, either fromthe fossil record of single species such as thoseof Osmunda, Onoclea and Woodwardia (e.g. Roth-well and Stockey, 1991; Rothwell, 1996a; Phippset al., 1998; Serbet and Rothwell, 1999; Pigg andRothwell, 2001), or in whole pteridophyte £orasfrom their surviving cytology (Page, 1967b, 1973).Similarly, there may be little change in at leastsome generic a⁄nities with habitats throughtime. Examples certainly include Onoclea, Osmun-

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da and Woodwardia, which appear to have hadmembers associated closely with swamp habitatmargins 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); Equisetumwith similar habitats for at least as long (McIverand Basinger, 1989) or very much longer (Page,1967b, 1972a); Acrostichum, characteristic todayof (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 theCainozoic (Collinson, 2002-this issue); free-£oat-ing water ferns (Azolla and Salvinia) in freshwaterfacies 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 openand disturbed ground including ¢reburn sitesand volcanogenic terrains since at least Mid-Cre-taceous (Collinson, 1996, 2002-this issue; VanKonijnenberg-van Cittert, 2002-this issue). Morecontentious (Collinson, 2002-this issue) at presentis the claim (Poole and Page, 2000) of a probableEocene epiphyte of Polypodiaceous a⁄nity,though I maintain my conviction: if there arePolypodiaceae and there are trees, then there areepiphytes (though I do not dispute that additionalevidence of these in physical connection would bevaluable!). 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 thatthese complexities still confer great versatility,£exibility and adaptive e¡ectiveness, especiallythrough their abilities of exploiting an unusuallywide range of marginal habitat conditions. Fernshave, 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 notonly modern stocks (e.g. Wagner, 1954; Hau£erand Windham, 1991; Hau£er et al., 1995) but alsoon 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 alsobeen emphasised within the Pteridophyta from afossil perspective since the Palaeozoic (DiMicheleand Phillips, 2002-this issue), and a diversity ofhabitats has been occupied through the Mesozoic(Van Konijnenberg-van Cittert, 2002-this issue)and Cainozoic (Collinson, 2002-this issue). Allof these alternatives will have operated, perhapswith varying emphases and in varying degrees,between times of relative evolutionary quiescenceversus 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 ecologicalpotentials which can thereby be achieved (Page,1997a, 2000, 2002c). These same innate mecha-nisms and processes must have similarly occurredthroughout much of pteridophyte fossil history,opening similar ranges of adaptations and ecolog-ical potentials, as strategic elements of recurringpteridological 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 orhabitats, seeking their modern equivalents forcomparison. Particularly important recent synthe-ses have been made in this perspective by, forexample, Rothwell (1987, 1991, 1996a,b, 1999).The approach presented here is proposed as com-plementary to that which can be gained from thefossils themselves. It is argued that the modernfern ecologies help to point to a diversity whichcould (and probably did) exist in Pteridophyta atmany times in the past. Using the same strategiesas their modern analogues, ancient ferns, at manydi¡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 ofhabitat miches as wide as those seen today.

Acknowledgements

On practical aspects, I am grateful for thesupport 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 manypteridophyte and conifer experimental cultures forover more than 30 yr, and those at Oxford, UK,Brisbane, Australia, and Newcastle, UK, Univer-sities for extended periods before this. I am alsograteful to the Royal Botanic Gardens, Kew andthe Natural History Museum, London, for accessto herbarium materials, and to the LinneanSociety and Camborne School of Mines, Univer-sity of Exeter, for access to library facilities in theircharge. On scientific aspects, discussions in thelaboratory, the field and the glasshouse, with Dr.Trevor Walker, Clive Jermy, Dr. Heather McHaf-fie, Dr. Adrian Dyer and Dr. Richard Batemanhave been long-term stimuli to the overall devel-opment and progress of these studies and to manyof the ideas contained therein. Dr. HeatherMcHaffie (Edinburgh, UK) has kindly providedadditional pteridological comments and Dr. Mi-chael Proctor (Exeter, UK) ecological commentson the resulting manuscript. I am further gratefulto Dr. Margaret Collinson for her enthusiasm andsupport in helping to bring my neobotanicalconcepts into a palaeo-botanic arena, and to her,Dr. Kathleen B. Pigg and Dr. Paul Kenrick formany helpful and constructive comments on theresulting manuscript from a palaeo-botanic per-spective. This paper is dedicated to the memory ofthe 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, indiscussions and joint fieldwork, to the formationof some of the ideas included here.

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PALBO 2428 5-6-02


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Ecologivcal Strategies in Fern Evolution[1]