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

Ecological strategies in fern evolution:

a neopteridological overview
Christopher N. Page a;b;
Royal Botanic Garden, Edinburgh, UK
Cornwall Geological Museum, Penzance TR18 2QR, UK


Drawing inferences about the past from the ecology of living organisms is one of several approaches to
reconstructing palaeo-environments. Pteridophytes are a major component of fossil floras, but their use as
environmental indicators is constrained as much by lack of ecological data on living species as by an understanding of
the distribution of fossils. Taking a neobotanical perspective, this paper discusses some important ecological strategies
of ferns and allied plants and their underlying selection pressures, based on an extensive survey of tropical and
temperate species and on horticultural experience of the behaviour of wild species in experimental cultivation. Broadly
parallel developments to similar selection pressures and environmental responses have been sought from amongst
distantly related extant families, to derive broad concepts of weaknesses and strengths inherent in the biology of these
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 architecture

b Slow plant growth rates

b Intolerance of widely fluctuating conditions

b Poorly controlled evaporative potential

b Uncontrolled high reproductive commitment

b Need to ‘return to the water to breed’

Advantages: b Low-light photosynthetic ability

b Diverse phytochemical armament

b High disease resistance under saturated humidity levels

b High tolerance of acute nutrient disequilibrium substrates

b High migrational ability of the airborne spore

b Spore tolerance of adverse aerial environments

b Flexibility of breeding systems to match varying ecological opportunity

b Revivalist tendencies of certain gametophytes

b Potential longevity of resultant sporophytes

b Exploitation of mycotrophy

b Exploitation of potentials of polyploidy

b Biotic independence

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

0034-6667 / 02 / $ ^ see front matter 8 2002 Elsevier Science B.V. All rights reserved.
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It is argued that collectively these weaknesses and strengths provide a broad framework, which, operating in varied
combinations, limit or open opportunities for exploitation of a considerable array of ecological habitats by
Pteridophyta. Based on these data, several general ecological principles are developed. It is proposed that, through
time, such strategies are likely to have opened many pteridophyte habitat opportunities, though not all of these will
necessarily have left directly identifiable signals in the fossil record.
Modern fern ecological limitations and advantages are shown to occur across broad taxonomic spectra and many
are innate abilities of the plants. It is, therefore, argued that a similar general framework of weaknesses and strengths
is likely to have operated in the past, and thus have been of similar relevance in defining and promoting the ecological
achievements of the fossil pteridophytes in relation to selection pressures and consequent adaptations. This opens up
the potential to extrapolate from the modern ecology for interpretation of palaeo-ecology and palaeo-environments.
Examples of this potential are given for each limitation and advantage, where possible incorporating evidence from
the fossil record. 8 2002 Elsevier Science B.V. All rights reserved.

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

1. Introduction tered world-wide literature, both pure and ap-

plied. There are a wide variety of relevant data
Pteridophyta are a major component of fossil (e.g. from biochemical to biotic, from edaphic to
£oras. In interpreting environmental relationships climatic, and from physiological to genetic and
of these plants, we are faced, on the one hand, by mycological) which need careful evaluation and
a good and very long fossil record through a great sensitive interpretation. These data must be re-
diversity of global habitats. On the other hand, lated to direct observations of both whole fern
there are some 12 000 or more living species of communities and individual species niches in the
ferns alone (plus horsetails and clubmosses) in a ¢eld (especially in the wet tropics). Autecological
world-wide array of extant habitats. Of the living information is added from life-cycle observation
species, we have good world-wide morphological, in experimental cultivation. A synthesis of resul-
taxonomic and phylogenetic information bases, tant data is necessary against the taxonomic spec-
but we are only just beginning to ask questions trum to which it might apply today, with constant
about the more subtle aspects of their ecologies awareness of the areas likely to be of particular
and the reasons behind the adaptations and the palaeo-relevance. It is also vital to be aware of
architectures that we see. what is not known or has been inadequately
In comparing the living and the fossil, it is im- studied which, even in living ferns, is manifold.
mediately clear that there is much common This account focuses particularly on ferns,
ground. However, it is also clear that not every although relevant comparable data from other
palaeo-problem is necessarily answered by the liv- pteridophyte groups (horsetails and clubmosses)
ing plants, in the same way that not every prob- are added where appropriate and available. The
lem of origin of the living plants is necessarily account draws on nearly 40 yr of personal ¢eld
answered by the fossil record. Both ¢elds have ecological observations and experimental study of
their unique strengths, and provide complementa- ferns. Identi¢ed and itemised on the basis on this
ry approaches, between which information evidence are: (1) the intrinsic limitations to fern
bridges can help to add important additional in- ecological success (Section 2: Intrinsic limitations
terpretative elements. to fern ecological success) ; and (2) the important
To assemble even the baseline account of extant advantages imposed on pteridophytes by aspects
fern ecology presented here, it is ¢rst necessary to of their biology, which establish recurring strat-
construct a skeleton of ideas and proposals which egies of fern ecology, adaptation and survival
can be tested against evidence. It is then necessary (Section 3: The recurring advantaging strategies
to draw together information from a highly scat- of fern ecology, adaptation and survival). These

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

enable ferns, despite the limitations, to occupy otic origin, have varied. Furthermore, it is ac-
and succeed in a wide range of ecological niches cepted that not all habitat possibilities under
today. An example of this success is the forest which fossil taxa have existed necessarily still ex-
margin colony-forming fern like Pteridium (brack- ist. Many taxa are also now extinct (DiMichele
en) in Plate I. and Phillips, 2002). Nevertheless, it is proposed
Both the limitations and the strategies are di- that similar overall strategies are likely to have
verse. In de¢ning these, broadly parallel examples operated as regular features of palaeo-fern adap-
of ¢eld situations and responses have been docu- tation, in response to generally similar past selec-
mented from among members of unrelated fern tion pressures whenever palaeo-events and palaeo-
families (both Leptosporangiate and Eusporan- opportunities and constraints have promoted
giate) in multiple locations in response to similar these.
selection pressures. This provides a resource-rich
information base, which points to principles of
modern fern ecological survival abilities which 2. Intrinsic limitations to fern ecological success
have potential to translate into broader palaeo-
settings. A variety of intrinsic limitations to fern ecolog-
It is not suggested that all interactions between ical success handicap ferns today, and have prob-
fossil ferns and their palaeo-environments have ably always done so. Appreciation of these limi-
necessarily always been identical to those of to- tations is essential to an understanding of the
day, since selection pressures, especially of a bi- strengths of the ecological strategies, which have

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then been achieved despite them. Seven such fac- pressures would tend to work towards achieve-
tors are de¢ned here. Virtually all of these apply ment of some degree mutualistic equation of hab-
broadly to all fern groups although, inevitably, a itat tolerance. A few extreme cases are known
few (but usually only a few) species have adapted which serve to show a little of the range of com-
to circumvent the disadvantage of at least some of plexities which may become involved. These in-
these handicaps. This was probably also true in clude the occurrence of apogamy, which produces
the past. sporophytes without fertilisation (Walker, 1979),
delayed sex expression (Duran and de la Sota,
2.1. The handicap of an independent gametophyte 1996), occurrence of clonal gemmiferous gameto-
stage phytes (Dassler and Farrer, 1996), and occurrence
of pH metamorphosis between gametophyte and
Restrictions imposed on the sporophyte by the subsequent developing sporophyte in Pteridium
occurrence, in the life cycle, of an independent (Page, 1986). In ferns with independent gameto-
gametophyte stage are at least twofold: phyte stages, marked contrast exists between the
(1) Collectively, the successful arrival, germina- ecologies of the gametophyte and sporophyte
tion, and establishment stage provides an ‘achilles (Farrar, 1967, 1985; Peck et al., 1990; Rumsey
heel’ to the whole fern life cycle, and is probably et al., 1992; Rumsey and She⁄eld, 1996).
the stage at which the greatest numbers of indi- Consequences may include enabling species to
viduals (by an order of magnitude) fail and be- survive under conditions which are at times un-
come eliminated on a regularly recurring basis in suitable for sporophyte formation or sporophyte
the ¢eld. survival (see also Section 3.11: Exploitation of
(2) Among the few successful establishees, the potentials of polyploidy). Such potentials, which
resulting gametophyte determines the general site can be far from ‘textbook’, need to be borne in
of origin of the sporophyte, whether this be opti- mind in the interpretation of the breadth of pte-
mal or not for the subsequent vascular genera- ridophyte adaptation, especially to more unusual
tion. palaeo-habitats.
High and fortuitous roles of chance and sharp
levels of selection pressures would seem to pro- 2.2. Single growing-point limitations of sporophyte
foundly characterise these normally short-lived architecture
stages of the fern life cycle, while the process of
fertilisation itself is also dependent of the addi- In great contrast to the multi-growing points of
tional presence of adequate free-water (see Section many angiosperms, the single growing-point of
2.7: Need to ‘return to the water to breed’). Be- the pteridophyte rhizome (whether it is a terres-
tween such very di¡erent organisms as the non- trial or aerial ‘stem’) becomes the whole basis for
vascular prothallus and free-living vascular spo- the origin and direct tenure of not only roots but
rophyte, it would seem likely that evolutionary also all leafy and fertile parts of ferns. Consider-

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

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able vulnerability is consequent should that grow- negotiate round or through this ‘skirt’ (Page and
ing point become damaged, and this basic archi- Brownsey, 1986).
tecture can also limit the £exibility of morpholog- Such crown vulnerability will have been char-
ical response (Gureyeva 2001). Additionally, acteristic of ferns through the whole of the fossil
damage response, through development of new record, through which similar (and perhaps other)
lateral growing points as side-rhizome out- strategic avoidance mechanisms will have been
growths, is usually slow. Main avoidance mecha- elaborated. The presence of either exceptionally
nisms, which at least partly circumvent this innate clean trunks to fossil tree ferns or the presence
vulnerability, include: of persistent tree fern skirts would itself indicate
(1) physical structure : this includes density of defensive mechanisms against the presence of
hairs, scales and occasional spines to protect the climbers or epiphytes in the associated palaeo-
young expanding croziers ; £ora. It would seem that the Palaeozoic tree
(2) removal of growing points to high above the fern Psaronius used neither of these deterrents ef-
ground, such as in tree ferns: this avoids tram- fectively as it was colonised by both epiphytes and
pling and direct foraging interest especially by climbers (Ro«ssler, 2000; DiMichele and Phillips,
small- to medium-sized tetrapods; 2002-this issue) though these may have been re-
(3) branching of the rhizomes : this provides stricted to the lower part of the trunk.
multiple rhizome-apex survival opportunities ;
(4) concentration of great species diversity in 2.3. Slow plant growth rates
sites of low browsing (and trampling) encounter :
¢de the great success of lithophytes and epiphytes Sporophyte (and sometimes gametophyte)
among ferns; growth rates can vary widely between di¡erent
(5) high emphasis on biochemical armament ap- fern groups, speci¢c taxa, parents and allopoly-
parently e¡ective against a broad-spectrum of an- ploid o¡spring (see Section 3.11: Exploitation of
imal taxa: see Section 3.2: Diverse phytochemical potentials of polyploidy). They can also vary in
armament. relation to location and habitat positioning within
In the case of tree ferns, particular vulnerability the same species (e.g. Cousens, 1981). Neverthe-
then ensues from the creation of a trunk which is less, in comparison with many angiosperms, over-
itself a desirable habitat for colonisation by other all fern growth rates are relatively slow (least so in
plants, notably by climbing epiphytes and scram- some epiphytes and some pioneer species), and
bling lianes. All of these are harmful to tree ferns this has been suggested to be linked to the inher-
since the inevitable upward growth of each is ently slow rates of some physiological processes in
drawn directly towards the single monopodial ferns (Raven, 1977, 1984, 1985a). These include,
tree fern crown. Further architectural develop- water movement in the xylem of purely tracheid-
ments by the tree fern are needed to counter these based construction (Woodhouse and Nobel, 1982;
advances. Two methods are adopted widely by Gibson et al., 1985); di¡usive resistance (Wong
existing tree ferns. Some produce fast upward and Hew, 1976) and conductance of photosyn-
growth resulting in a slender trunk which itself thetic carbon assimilation in mainly C3 pterido-
has a smooth polished surface (with clean frond phytes, which are considered ‘‘generally towards
abscission leaving only smooth leaf scars) upon the low end of the range’’ for terrestrial tracheo-
which it is di⁄cult for climbers to gain purchase. phytes (Raven, 1985b).
Others, such as Dicksonia (Plate II, 1) and some Constraints imposed by growth rates in associ-
members of the Cyatheaceae and Blechnaceae, ation with the pteridophyte life-cycle (see Section
have slow upward growth (resulting in a thicker 2.1: The handicap of an independent gameto-
and more rough-surfaced root-clad trunk), but phyte stage) also limit the capacity of pterido-
they retain dense ‘skirts’ of old fronds hanging phytes to adopt short life-cycle turnovers of the
below the crowns. These act as a foil to ascending type which have enabled mosses as well as £ower-
climbers and epiphytes which substantially fail to ing plants to evolve small ephemeral forms (Ra-

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ven, 1985b; Richardson, 1992, p. 98). This is sup- ment, such as on emerging, to habituation to am-
ported in conditions of experimental cultivation bient environmental conditions: light regimes,
where only a few exceptional examples have moisture levels, air movement rates (Page, person-
been met which display rapid life-cycle turnovers al observations). Expanding fronds adapt to these
of the order of a year or less from spore-sowing to at the levels at which these environmental in£uen-
sporophyte ¢rst spore production. These occur in ces are met on initial frond expansion. Should
a few ‘modern’ genera (such as Anogramma and conditions subsequently change (such as increase
Pityrogramma (both Gymnogrammaceae) and in light levels due to a tree fall gap forming in the
Doodia (Blechnaceae)) and represent under 0.2% canopy) existing fronds appear unable to re-
of taxa personally cultivated in 40 years. Annuals adapt. Only subsequently emerging fronds adapt
are thus rare in pteridophytes as a whole, and the as far as they are functionally able to the new
very great majority of ferns are thus committed conditions encountered. Plants may require a
perennials, with inherently longer life-cycle turn- full growing season before all fronds borne be-
overs (and often years to maturity) that this im- come modi¢ed to any major features of environ-
plies. mental change. Furthermore, lack of stomatal
Such multi-year perenniality seems likely to control, should conditions change, has been docu-
have also been the case for most ferns in the mented in Lycopodium species, with modest
past. Furthermore, there is also a general trend amounts of inter-speci¢c variation (Heiser et al.,
for greatest longevity to be achieved amongst sev- 1996).
eral taxonomically more ancient extant taxa (e.g. Established sporophytes thus do not respond
Osmunda, Angiopteris, Equisetum), which may well to environmental £uctuations, unless they
mean that longevity may have been an even great- are ones to which a species is especially pre-
er feature of even more pteridophytes in the fossil adapted. It is probably such inherent incapabil-
record. That this is usually coupled to ultimate ities of short-term response that ensures that
size achieved should allow for appropriate fossil fern sporophyte success is always greatest when
signals to be identi¢ed and perhaps community environmental conditions (of virtually all types)
age-structure to be indicated, and might further remain most constant.
indicate palaeo-sites of adequate habitat stability As a widely encountered example, it is almost
(see also Section 2.4: Intolerance of widely £uc- certainly for these reasons that, in temperate cli-
tuating conditions). Occurrence of multi-aged mates, fronds are delayed in emergence until the
populations, including aged individuals, would tree canopy itself has mostly completed growth
imply continuing habitat stability, and where re- (Page, 1988). Little would be achieved, and there
inforced by representation within the same com- is everything to loose, by timing frond-expansion
munity of high taxonomic and morphological di- to be any earlier than this. In tropical moist cli-
versity, would clearly indicate climax palaeo- mates, however, where there is year-round forest
communities with multiple niche opportunities. canopy shade-provision, new fern frond growth
This seems to have been the case for some Palaeo- can occur throughout the year. By contrast to
zoic marattialean communities (DiMichele and the single spring growth ‘£ush’ of fern frond
Phillips, 2002-this issue). emergence of temperate regions, tropical fern
fronds arise typically in a steady and sequenced
2.4. Intolerance of widely £uctuating conditions year-round succession, accommodating ample op-
portunity for subsequent adaptation to any envi-
Intolerance by unadapted sporophytes of ronmental changes which do arise. Other varia-
widely £uctuating conditions is a particularly tions occur in tropical dry climates, and in all
under-appreciated ecological limitation of the ma- sites, further micro-habitat variations appear to
jority of ferns (Watt, 1976; Arens and Baracaldo, be involved. An interesting tropical example, The-
2000). Fronds of most extant ferns (perhaps all), lypteris angustifolia, is being very closely docu-
appear to be able to make a once-only commit- mented by Sharpe (1996), in which seasonal rain-

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fall patterns are closely re£ected in subsequent In Equisetum, Equisetum £uviatile tolerates the
development patterns of the plant. Such patterns most anaerobic (and still) water conditions, while
may well have considerable bioindicator value, at the other extreme, Equisetum telmateia requires
and need more detailed study. the most oxygenated water, and is indicative of
If this fern preference for constant environment constantly moving water sites (such as especially
also prevailed in the past, as seems likely, then that below springlines Page, 1988, 1997b). Such
palaeo-environmental conditions can be inferred aspects of micro-habitat di¡erences must also ap-
from fossil fern £oras. For example, fern crowns ply to many pteridophytes in other sites.
with fronds and frond buds simultaneously at Climatic factors especially closely in£uence
multiple stages of development (either on individ- pteridophyte success and di¡erentiate closely be-
ual specimens or within populations) would be tween that of di¡erent fern species. These include,
usefully indicative of stability within a growing- in particular, such factors as frequency of precip-
season (and could lead to an estimate of growth- itation and its temporal distribution (i.e. not just
season length, such as in the wet tropics today). overall amount), degree of exposure versus shel-
By contrast, frond buds simultaneously at the ter, and factors linked more indirectly to evapo-
same stage would indicate growing-season release ration such as cloud-cover. There is, as yet, re-
within a more seasonally £uctuating environment. markably little accessible data on most of these
A further signal reinforcing the latter, but in the aspects even for living pteridophytes. It requires
non-growing season, might be the additional pres- diligent e¡orts to draw such information together
ence of seasonally developed subterranean storage even for well documented areas such as Britain
organs. Root tubers on some ferns (e.g. Adian- and Ireland (see, for example, maps of several
tum), if fossilised, would indicate dislodgement factors especially signi¢cant to pteridophytes gen-
during a dry-season interval. Equisetum, where erated on long-term accumulated data by the Brit-
clearly fossilised with tubers, would indicate fos- ish Meteorological O⁄ce in Page, 1982b).
silisation in winter (between September and early There is considerable potential to exploit pter-
April in the northern hemisphere), and that the idophytes as discriminating and sensitive environ-
aerial parts would have been deciduous and thus mental indicators, both for the present and the
not simultaneously present. past, using approaches being more widely devel-
oped (and funded!) mainly by agro-meteorologi-
2.5. Poorly controlled evaporative potential cal and forestry sources (see especially Thompson
et al., 2000). Fern £oras and nearest living rela-
The general need for moist environments, with tives (‘indicator species’) could both be applied in
low evaporative potentials to counter high rates palaeo-environmental studies. Environmental in-
of water loss, characterises much of the life-cycle dicators could be used, for example, for establish-
of the majority of ferns (e.g. Wylie, 1948). This ing relative comparisons between habitats and
problem places often severe limitations on the de- niches in separated palaeo-locations (cf. the mod-
gree of exposure which can be tolerated by many ern Equisetum example cited above).
ferns. Such poor control clearly restricts pterido-
phyte and especially fern success on both a re- 2.6. Uncontrolled high reproductive commitment
gional and a habitat basis, and is certainly also
highly taxon-speci¢c. It is a noteworthy aspect of Nearly all pteridophyte sporophytes, including
this limitation in living fern taxa, that individual ferns of most genera, have a high and largely un-
species are often limited by particular levels of controlled annual reproductive commitment.
soil-water availability, as well as surrounding air Once an appropriate stage of maturity for an in-
humidity. Furthermore, even within the same dividual sporophyte has been reached, spores are
habitat, di¡erent species can have subtly di¡ering typically produced in prodigious numbers
requirements, including lateral movement and throughout the remaining life of the plant. This
particular aeration levels of the soil water present. may be over decades or more (Gureyeva 2001).

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As a consequence of this production rate, extra- is thus limited to occasions and locations when
ordinary levels of over-saturation must regularly such free water exists. Observations in experimen-
occur in terms of what is necessary to maintain tal culture (Page and Walker, independent person-
individual populations within existing commun- al observations) show that for some species this
ities, where the great majority of spores must in- may be as ¢nely tuned as speci¢cally timed an-
evitably fall (e.g. Conant, 1978; Dyer and Lind- therozoid release (and perhaps archegonial recep-
say, 1992; Bernabe et al., 1999). The price of such tivity) over only certain periods in seasonal and
over production, and the inability of most ferns to even diurnal cycles, with which such free water
control it, must be a considerable drain on recur- has to necessarily coincide. This is a little-appre-
rent energy commitments by the parent sporo- ciated factor which may well contribute substan-
phyte. These levels of commitment, the apparently tially to detailed delimitation of pteridophyte
highly sacri¢cial nature of much of the process, niches, habitats and overall ranges, as well as hy-
and the fortuitous roles of chance are probably brid occurrence (and thereby evolutionary success
little di¡erent in character today from those which (see Section 3.11: Exploitation of potentials of
typi¢ed the life histories of ferns through their polyploidy).
long palaeo-history. In this respect, the Pteridophyta as a whole are
This disadvantage is, however, a two-edged very much the plant Kingdom’s equivalent of the
sword, since some clear advantages may well also Amphibia, between which there are many broad
be gained by large spore numbers. These are dis- similarities in ecology, life-style, tropical diversity,
cussed in Section 3.5: High migrational ability of habitat range, moisture limitations and the con-
the airborne spore. Of these, signi¢cant in a pa- tinuing occurrence of a free-living ‘juvenile’ phase
laeo-perspective are likely to be combinations of (Page, 1985). Such similarities and limitations
recurrent arrival at sites of poor access, abilities of must have applied at least equally strongly
potentially long-distance dispersal, and of rapid throughout the pteridophyte fossil record, where
exploitation of sites immediately following post- other pteridophyte^amphibian analogues might
disaster scenarios. All, and especially the latter, also exist.
open opportunities for serial successions to begin Clearly, for almost all pteridophytes, the achilles
to involve pteridophyte sporophytes from the ear- heel of a free-water requirement will have been
liest stages, in potentially large numbers. These experienced throughout their past history, to the
have, through the fossil record, doubtless greatly degree that fossil pteridophyte presence is neces-
in£uenced the overall ability of pteridophytes sarily indicative of the presence usually moist en-
(and especially ferns) to become exploiters of the vironments, in which adequate free-water (chie£y
epiphytic niche. However, this may seldom be a by precipitation) will at some time have been
habitat of high preservation potential (Poole and present. To a large extent, pteridophyte taxonom-
Page, 2000) and is hard to document in the past ic and morphological diversity today is a measure
(DiMichele and Phillips, 2002-this issue). of the regularity and reliability of occurrence of
such water ^ ¢de the overwhelming abundance
2.7. Need to ‘return to the water to breed’ which ferns can achieve in the regularly moist
cloud zones of tropical mountain mist forests to-
The need for the existence of free water, even if day. (This limitation clearly links closely to that
only as a ¢lm, is essential for sexual fertilisation of Section 2.4: Intolerance of widely £uctuating
by free-swimming motile antherozoids within the conditions, and Section 2.5: Poorly controlled
immediate habitat niche in which the prothalli of evaporative potential, and also to Section 3.3:
the gametophyte generation actually grow. Apart High disease resistance under saturated humidity
from in the example of occasional apomictic ga- levels). Sites of exceptional fern diversity within
metophytes (see Section 3.7: Flexibility of breed- the fossil record, coupled with analysis of the eda-
ing systems to match varying ecological opportu- phic niches occupied by the species and life-forms
nity), reproduction for most pteridophyte species involved, can potentially provide a valuable tool

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towards determining aspects of water availability very many, e.g. Plate II, 3) exploit a niche in
in various palaeo-environments. which competition pressure today is substantially
reduced. These abilities undoubtedly greatly facil-
itate the occupation of a wide range of niches in
3. The recurring advantaging strategies of fern forests, from deep shaded ravines to dark forest
ecology, adaptation and survival £oors, as trunk epiphytes and climbers, and as
plants of highly cloudy or frequently misty envi-
In contrast to the seven limitations above, the ronments. Low light-saturation e⁄ciencies will
advantaging strategies of fern ecology (12 are have been a particularly important factor through
identi¢ed here as 3.1^3.12) are the ‘positive’ side the course of angiosperm radiation (e.g. Crane,
of fern potentials, adaptation and survival. These 1987). Such shade-tolerating potentials have al-
compliment those of the ecological approach of most certainly been available to ferns in habitats
Grime (1977, 1985). These strategies re£ect recur- of earlier forest types too (e.g. Thomas, 1985) and
ring pteridophyte strengths today and are likely to could well have evolved, for example, as adapta-
have done the same throughout the history of tions to highly cloudy and misty environments,
pteridophytes. very long before angiosperm diversi¢cation.
In deriving an analysis of these strategies, the Probable forest-£oor shade tolerant taxa (on
extant ferns provide a resource-rich information the basis of their nearest living relatives) are
base, in which laboratory work and experimental known in some palaeo-£oras (e.g. Rothwell et
cultivation each contribute a substantial experi- al., 1994; Stockey et al., 1999). Large and delicate
mental database. The evidence is combined here fern fronds are also represented in the fossil rec-
with information from the ¢eld to achieve an ord (e.g. Deng, 2002-this issue) and so are ferns of
overall broad ecological synthesis. The evidence the shaded woody habitats of peat-forming
supports the view that many clear and de¢nable swamps (Collinson, 2002-this issue; DiMichele
principles of survival exist amongst extant fern and Phillips, 2002-this issue; Van Konijnenberg-
taxa, governed by innate abilities of the plants van Cittert, 2002-this issue). However, ferns of
themselves, and which occur across broad taxo- shade habitats are, from evidence of living species,
nomic spectra. frequently soft and/or thin-fronded and of gener-
ally delicate texture. Plants of such structure (es-
3.1. Low-light photosynthetic ability pecially extremes like Hymenophyllaceae) would
seem to o¡er a particularly low potential to nor-
Virtually all observational fern ecology today mally become well-represented (at least as macro-
would support the view that many ferns survive fossils) in most fossil £oras. By contrast, the
particularly well in levels of light which are too coarser-textured often higher biomass, tough
low for most competing angiosperms (as well as structures (especially stipes) and frequently more
many conifers) to tolerate, but I am aware of few monospeci¢c counterparts (e.g. Plate I) of more
exacting physiological measurements which ad- open habitats have higher fossilisation potential
equately quantify this. Complete photosynthetic (e.g. Collinson and Ribbins, 1977; Yao and Tay-
saturation at low levels of incident light would lor, 1988; Skog, 1992; Rees, 1993; Gandolfo et
appear to be the key factor (Page, 1979b). Arina- al., 1995; Cantrill, 1996). (Today, these ferns in-
wati et al. (1996), for example, quote high total clude genera such as Dennstaedtia, Lonchitis, His-
chlorophyll levels and particularly low light-satu- tiopteris, Hypolepis, Paesia, Pteridium.) This ta-
ration photosynthetic rates of fronds of the trop- phonomic bias should be taken into account
ical climber Teratophyllum rotundifoliatum (which when interpreting fern £oras of the past.
has fronds in both low and high light levels), and
indicate that di¡ering in£uences of light type may 3.2. Diverse phytochemical armament
also be involved.
Fern species of low-light habitats (which are Mostly only becoming known in the last 25 yr,

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diverse phytochemical armament is probably the by cocktails of biochemical repellent pathways in-
most e¡ective and widespread strategy in promot- volving sometimes complex chemical components
ing direct vegetative survival of Pteridophyta as a (Bohm and Tryon, 1967; Hayashi et al., 1977;
whole. It is becoming clear that phytochemical Cooper-Driver, 1978, 1985; Balick et al., 1978;
armament, of widely di¡ering degrees and types, Jones and Firn, 1978, 1979; Gerson, 1979; Had-
is taxonomically widespread in ferns and other ¢eld and Dyer, 1986; Suksamrarn et al., 1986;
pteridophytes, and appears to be the prime anti- Smith et al., 1990).
herbivore grazing defence mechanism of both gen- Sporophytes of Bracken (Pteridium) have been
erations. more extensively studied in this respect than any
Such biochemical armament has clearly become other fern, and provide a valuable generic exam-
an e¡ective route of defence for such a predom- ple. Pteridium is known to contain a particularly
inantly herbaceous group with relatively slow formidable armoury of repellents, from tannins
growth rates (see Section 2.3: Slow plant growth and sesquiterpenoids to phenols and cyanide (as
rates), vulnerable growing points and organs and a cyanogenic glycoside), plus two carcinogens, a
lack of most other physical defences or herbivore leukaemiagen and, for good measure, a broad-
avoidance mechanisms (see Section 2.2: Single spectrum insect ecdysone. Collectively, or sepa-
growing-point limitations of sporophyte architec- rately, these can have dire e¡ects on potentially
ture). It probably also contributes substantially to browsing animals of many types (e.g. Harding,
the survival of gametophytes, and thus to mitigat- 1972; Cooper-Driver and Swain, 1976; Evans,
ing against the apparent vulnerability of this free- 1976, 1986; Hendrix, 1977; Temple, 1981;
living stage (see Section 2.1: The handicap of an Schreiner et al., 1984; Fenwick, 1988; Had¢eld
independent gametophyte stage). Such biochemi- and Dyer, 1988; Saito et al., 1989; Galpin et al.,
cal armament, however, undoubtedly requires 1990; Low and Thomson, 1990; Smith et al.,
continuing resource and energy commitments on 1990; Wells and McNally, 1995; Bronstein,
the part of the plant, but it avoids the need for 1998; Thomson, 2000). Allelopathic compounds,
development of elaborate physical defence struc- toxic to other plant growth, are also copiously
tures, thus enabling relatively simple pteridophyte produced by bracken (e.g. Gliessman, 1976;
architectural form to persist. Gliessman and Muller, 1972) and probably by
Nevertheless, remarkably little is yet under- many (? most) ferns (Weinberg and Voeller,
stood about which of any known phytochemical 1969; Banerjee and Sen, 1980). Furthermore, at
substances are employed to achieve e¡ective de- least in Pteridium, the spores also are known to be
fence and exactly what they are targeted against. substantially armed with some of the same com-
Currently we are only aware that present targets pounds in even higher concentration per dry
seem broad, and were probably similarly so in the weight than in the vegetative body of the plant
past. Field botanists will be aware, however, that (Evans and Galpin, 1990). These compounds are
few modern ferns usually show signs of any sig- presumably e¡ective against sporophagy during
ni¢cant herbivory in the ¢eld. Even to a human both pre-dispersal and post-dispersal phases.
nose, many ferns have distinctive (and often spe- Fern fronds can and do, however, provide
cies-speci¢c) odours (e.g. Plate II, 2), some of roosting-habitats for a great number of terrestrial
which are quite curious: e.g. the temperate Gym- arthropods (e.g. Lawton, 1976; Gerson, 1979; Ot-
nocarpium robertianum (Athyriaceae) which has toson and Anderson, 1983; Lawton and MacGar-
an apple-like fragrance, Polypodium glycyrrhiza vin, 1985; Brown, 1995; Jensen and Holman,
(Polypodiaceae) which smells of liquorice, and 2000) with which the plants appear to successfully
the tropical Anemia phyllitidis (Schizaeceae) which co-exist. A limited tolerance to a degree of grazing
smells to me of running model railways !). The appears to exist between ferns and some insects,
research which is available suggests that, in most notably Lepidoptera and sometimes Hemiptera
ferns, general browser interest appears to be suc- (Balick et al., 1978; Lawton, 1982; Lawton and
cessfully checked (or at least, held to a minimum) MacGarvin, 1985; Weintraub et al., 1995). Addi-

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tionally, various ant^fern associations and mutu- indicates a high probability that such defences
alisms are becoming recognised (e.g. Darwin, are general in most living pteridophytes. They
1877; Southwood, 1977; Page, 1982a; Lawton can be varied (e.g. through a number of di¡erent
and Heads, 1984; A.F. Tryon, 1985; Walker, secondary compounds focussing especially,
1985; Arens and Smith, 1998). Sometimes further though not exclusively, on a diverse range of cy-
defensive bene¢ts to the plant may be gained by clopropane compounds ^ Potter, 2000) and pro-
tolerating the presence of such animals, and some mote, amongst other e¡ects, onset of degenerative
defence mechanisms, expensive in energy invest- conditions in a broad spectrum of animals expe-
ment, may be discontinued when not needed. riencing them. Other contained compounds, such
An example of this is in the specialist myrmeco- as ecdysones, are more arthropod-speci¢c.
philous epiphytic Lecanopteris carnosa (Polypo- Also essentially phytochemical in origin (and
diaceae). Experience in glasshouse cultivation almost worthy of a separate entry as a further
(Page and Walker, personal observations, 1964^ independent advantaging attribute of ferns, were
1967) shows that this species has prothalli and there clearer evidence), is the occurrence in ferns
young sporophytes which are especially attractive of chemically unusual intra-cellular cements,
to rapid and usually terminal depredation by which bind cells together (Manton, 1950). As far
small slugs. However, in the wild, this species is as I am aware, in contrast to all phytochemically
regularly and aggressively ant-colonised (and is toxic aspects of ferns, nothing is known about
here inferred to be likely to be mutualistically these, beyond that they contrast with those of
ant-protected) on the branches of the tropical all £owering plants. In ferns, these have the repute
lowland swamp-margin trees on which these large of not being soluble in hydrochloric acid, and of
epiphytes normally grow (Jermy and Walker, hence making fern frond material indigestible to
1975). It is presumed here that chemical defences all animals dependent on an HCl-mediated diges-
have been dropped when other alternative (less tive system. Indeed, slugs and snails are the only
energy-consuming) defence mechanisms have be- animals known (at least by repute amongst pter-
come available. Our observations showed that the idologists) to have the necessary stomach enzymes
same slugs and snails did not similarly attack a with which to attack these fern cements. I person-
broad range of other adjacent fern cultures. This ally regard this as a potentially important survival
provides at least some negative evidence of a nor- strategy in ferns (and possibly in other pterido-
mal defence in most pteridphytes (presumably phytes) against animal depredation, but, so far
chemically mediated) which would appear to be as I am aware, the whole topic appears virtually
sensed, and thus avoided, by slugs, snails and pre- unresearched. It could, however, have consider-
sumably other invertebrates. able implications both for the survival of ferns
Some of the e¡ects of pteridophyte chemical against a range of herbivores through time. Fur-
constituents today are responses to potential mi- thermore (especially if it also operated against de-
crobial attack (e.g. Kobayashi et al., 1975; Baner- cay organisms ^ I do not have any evidence either
jee and Sen, 1980). However, it is mainly against way), it may also have a¡ected the preservation
browsing pressures, especially by arthropods (e.g. potential of ferns throughout the fossil record.
Wootton, 1981, 1990; Scott et al., 1985, 1992, Pteridophytes as a whole have been the focus of
1996) that selection pressures for the development general browsing attention (including detritivory)
of such a diverse array of phytochemical arma- especially from invertebrates (such as Oribatid
ment (and a diversity of arthropod counter-mea- mites ^ Labandeira et al., 1997) since the Carbon-
sures) will have been recurrently stimulated. Very iferous or earlier (e.g. Scott and Taylor, 1983;
few other ferns have been studied in any compa- Jeram et al., 1990; Stephenson and Scott, 1992;
rable detail to Pteridium, although the list of taxa Scott et al., 1985, 1992, 1996; Jarzembowski,
and known phytochemical isolates and their di- 1994; Collinson, 1996; Labandeira and Phillips,
versity of e¡ects on modern browsing animal 1996; Labandeira, 1998). There are some indica-
groups is steadily growing. The extent of these tions, from Palaeozoic compression £oras, that

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fern leaves were already then less browsed than gimes within which most £owering plant seedlings
alternative vegetation (e.g. Beck and Labandeira, would readily ‘damp-o¡’ through rapid fungal at-
1998; Collinson, 1996, p. 380^381) and, although tack. Cultivation experience shows that intrinsic
the Palaeozoic tree fern Psaronius exhibits a host pathogen resistance abilities are taxonomically es-
of arthropod interactions these do not seem to pecially widespread in ferns and are expressed ef-
include leaf-feeding (Labandeira, 2001). During fectively in both the gametophyte and the sporo-
this long period of interaction, evolutionary pres- phyte stage to the great competitive ecological
sures for the development of adequate armament advantage of the fern. Extreme examples must
must have been intense, constant and diverse in be the ¢lmy ferns (Hymenophyllaceae), many of
most habitats in which Pteridophyta have suc- whose members grow permanently and success-
ceeded. Clearly modern ferns enjoy considerable fully in habitats such as the spray-zones of trop-
abilities to achieve complex biochemical defence ical waterfalls, where the £imsiness of the fronds
potentials (e.g. Hartzell, 1947; Evans and Mason, (Plate II, 4) might appear to scarcely make a side-
1965; Hayashi et al., 1977; Swain and Cooper- salad for a self-respecting pathogen! The mecha-
Driver, 1981; Ojika et al., 1987; Saito et al., nisms of such tolerance are very little understood,
1989; Kushida et al., 1994; Castillo et al., 1997; though antibiotic e¡ects have been reported in
Potter, 2000; Siman et al., 1995, 2000). Doubtless ferns (e.g. Kobayashi et al., 1975; Banerjee and
many other variations have occurred through the Sen, 1980).
fossil record against the same selection pressures. Thin-fronded ‘¢lmy ferns’ (which have been as-
Increasingly, evidence is that the pathways of signed to the Hymenophyllaceae) are known from
known defence involved are, chemically speaking, the Mesozoic (Deng, 1997; Axsmith et al., 2000)
complex; biologically speaking, e¡ective; and implying a long history for ferns growing in satu-
evolutionarily speaking, diverse and often subtle. rated humidity levels. Signi¢cantly, many of the
The main measure of the speci¢c e⁄cacy of bio- ferns in a diversity of distantly related families in
chemical defences through the fossil record is this habitat today are successfully bulbiferous,
most likely to be gained through assessments of often developing a ‘walking-fern’ habit and/or de-
actual recordable incidences (and hence inferred velop axillary branching patterns of growth. Such
susceptibility) of browsing activity (foliar/spore) habits occur in few other habitats, and hence
between contemporaneous taxa and through would provide an important marker in the fossil
time (like that of Wilf and Labandeira (1999) record for such humidity and moisture regimes.
for angiosperms). Unfortunately, for the fossil
record, those taxa which were highly susceptible 3.4. High tolerance of acute nutrient disequilibrium
will be those least likely to be represented. How- substrates
ever, clearly the Pteridophyta are not mere begin-
ners at these diverse and extensively practised Two suites of factors here (which could almost
achievements! rank as separate advantaging strategies in their
own right) operate either independently or collec-
3.3. High disease resistance under saturated tively in achieving unusually high and varied nu-
humidity levels trient disequilibrium tolerance amongst modern
Once past the life-cycle hurdles of spore surviv- These suites are: (1) a direct ability to tolerate a
al (including possible survival as soil spore-banks range of exceptionally low nutrient terrains (e.g.
^ see Dyer and Lindsay, 1992), potential sporoph- Plate II, 5); (2) an additional ability to tolerate
agy (e.g. Leschen and Lawrence, 1991) and additional unusual levels of excess mineral ele-
achievement of successful germination and estab- ments which can also be present in some of these
lishment (see Weinberg and Voeller, 1969; Dyer, terrains, and which can be at levels that would be
1979; Lloyd and Klekowski, 1970; She⁄eld, 1996 toxic to many other plants (e.g. Plate II, 6).
for reviews), ferns succeed under humidity re- Field ecology suggests that these tolerances ap-

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

pear to be possessed, either separately or collec- ised horticultural compost media (including,
tively, within an especially wide taxonomic array ironically, most epiphytes, providing that they
of genera and families of extant ferns (e.g. Con- are not over-fed with standard nutrient additives).
way and Stephens, 1957; Kruckeberg, 1964, 1976, This indicates that the often high localisation of
1964, 1976, 1984; Holbrook-Walker and Lloyd, forest species in the ¢eld is not purely (or even
1973; Lloyd, 1976; Kornas, 1978, 1985; Page, mainly) the result of narrow mineral tolerances
1979b, 1988, 1999; Sleep, 1985; Spicer et al., and speci¢cities (beyond the general one of epi-
1985; Malaisse et al., 1994; Tsuyuzaki, 1997). phytes). Instead, the niche-width of these in the
Within each suite, wide and diverse spectra of wild (often extremely narrow, sometimes also
actual tolerance levels and types doubtless exist. highly localised) is mainly prescribed by overrid-
In the second suite, wide variations in the individ- ing interactions of immeasurably subtle, complex,
ual minerals which can be tolerated almost cer- and highly pervasive, biotic competition.
tainly exist, although beyond ¢eld observations, By contrast, ability to succeed on more gener-
there is yet little available quanti¢ed data on alised terrains with lowered (or initially virtually
this. Amongst the ¢rst suite, subtle di¡erences zero) biotic competition can open wide habitat
amongst tolerances of epiphytic taxa are re£ected opportunity for those species which are able to
in the tendency (in the tropics especially) for dif- achieve high tolerance levels of the ruling nutrient
ferent pteridophyte epiphytes either to be general- disequilibriums. For these, the edaphic speci¢city
ist or more narrowly specialist species as far as can seem very high. Yet many pteridophytes
preferred host-tree habitat selection is concerned which are vigorous (sometimes to the extent of
(cf. Gardette, 1996). Signi¢cantly, in both suites, being rampant) in edaphically low-nutrient habi-
species with di¡erent apparent substrate preferen- tats in the wild (notably, for example, many Ly-
ces (presumed a re£ection of di¡erent tolerances) copodiaceae, virtually the whole of the Gleiche-
frequently occur within the same genus. This sug- niaceae and Lindsaceae, Dipteridaceae, Matonia
gests that the detailed tolerances have evolved and Christensenia, and most Schizaeaceae) can,
very numerous times in ferns, adapting individual ironically, prove extraordinarily di⁄cult to grow
taxa closely and subtlety to e¡ective exploitation at all in conditions of experimental cultivation !
of particular local habitat opportunities. Extremely high and exacting directly edaphically
There are strong contrasts between the ability limited tolerances and limitations seem indicated
to succeed in the ¢eld on generalised, open, but for such pteridophytes.
strongly limited terrains versus (at the extreme Both suites of this nutrient disequilibrium tol-
opposite) within exuberant mature mesic forest erance strategy, either separately or in combina-
vegetation. These contrasts emphasise the roles tion, advantage ferns in enabling them to grow in
of physical/chemical versus biotic pressures with a wide range of sites which are either too nutrient-
which respective pteridophytes are confronted. poor or are too high and toxic in unusual (e.g.
Mature forest vegetation, and especially rain- metalliferous) elements for most other competi-
forest, is widely appreciated to be a very complex tors to succeed equally well. The net e¡ect of
community, within which niche preferences be- these abilities is to open a variety of low-competi-
tween fern species are almost certainly very pre- tion habitat opportunities for colonisation into
cisely and exactingly di¡erentiated (e.g. Page, sites which can be widely available to pterido-
1979b, 1988; Petersen, 1985; Cousens et al., phytes because of the migratory e⁄ciency of the
1988; Young and Leon, 1989; Van der Wer¡, airborne spore (see Section 3.5: High migrational
1992; Tuomisto and Ruokolainen, 1994; Poulsen ability of the airborne spore). Typical habitat ex-
and Neilsen, 1995; Poulsen and Tuomisto, 1996; amples include:
Tuomisto and Poulsen, 1996). Most pteridophyte b intrinsically nutrient poor sandy heathlands

species from such sources can be successfully and savannahs;

reared in glasshouse culture (personal observa- b the leached soils of constant light rainfall

tions 1958^2001) on relatively arbitrary standard- conditions such as laterites and those of mountain

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saddles where conditions of constant downward usual degrees of tolerance levels from both suites,
water and nutrient movement apply (e.g. Dipteris, and the levels of such tolerances often appear to
Plate II, 5); be highly taxon-speci¢c. A smaller diversity of
b newly formed volcanic ash surfaces ; plant habits is present, with plants usually of
b post-wild¢re sites; small size, scattered (seldom contiguous) occur-
b erosion surfaces of lithophytic sites ; rence, and tough, leathery growth. Dead fronds,
b habitats of high metalliferous availability frond debris and especially frond bases may per-
such as ultrama¢c soils and man-made metallifer- sist around parent plants for years. On directly
ous mine spoils; nutrient poor edaphic sites, either characterised
b epiphytic habitats. by post-¢reburn environments or (especially) by
Wide arrays of fern species from diverse fami- erosion-regimes and constant surface moisture
lies are today specialist colonists of many of these downwash such as today on high-mountain sad-
sites, with considerable specialisations especially dles, notably sprawling and often rampant pteri-
of life-form between di¡erent fern families in ex- dophyte habits are especially characteristic, with
ploiting di¡erences between each of these rela- tough growth structure typically yielding much
tively demanding situations. local and outwash debris.
For example, epiphytic habitats almost exclu- The frequency of occurrence, and the taxonom-
sively require unusually high tolerance levels of ic diversity, of ferns in all of these habitats today,
the low-nutrition suite, and subtle levels of biotic with subtle di¡erences between sometimes related
competition are probably also involved in di¡er- taxa and their adaptations, suggests a long past
entiating between di¡erent ‘preferred’ epiphytic history for this phenomenon. Sites of unusual
substrates. Despite these limitations, an enormous mineral availability must have always occurred,
number of pteridophyte (especially fern) epiphyte while ¢reburn sites, some with ferns, are known
species exist. Some (e.g. species of Tmesipteris) are since at least the Early Carboniferous (¢de Scott
themselves specialists mainly of tree-fern trunks, and Jones, 1994; Falcon-Lang, 1998, 1999; DiMi-
even to genus (Dicksonia), while the majority even chele and Phillips, 2002-this issue). Volcanic ash
specialise in the occupation of speci¢c branch habitats, also with ferns, are known from at least
niche locations (often prescribed by their mor- similar times (Scott and Galtier, 1985; Brous-
phology) and tree canopy heights occupied on miche et al., 1992; Crowley et al., 1994). The
particular tree species hosts. The whole epiphytic antiquity of this strategy, which probably enabled
pteridophyte suite is composed of an enormous opportunistic colonisation even among early ¢li-
range of morphological habits of pteridophytes, caleans, is further indicated by Galtier and Phil-
from creeping to pendulous, and some quite bi- lips (1996). Epiphytism amongst ferns, although
zarre compost-making specialists. Many can to- very fragmentarily known (e.g. Sahni, 1931;
tally blanket portions of the bark of the tree on Rothwell, 1991; Poole and Page, 2000) has a
which they grow. Some appear physically inter- very long fossil history from the Palaeozoic (Ro«ss-
dependent, and some are symbiotically ant-asso- ler, 2000; DiMichele and Phillips, 2002-this issue).
ciated in obligate or facultative ways, or subse- Survival of ancient biota collectively on such
quently form various other animal and other pte- sites seems also indicated amongst extant taxa
ridophyte habitats. Typically they are (relatively) by the occurrence of taxonomically outlying and
fast-growers, and the duration of life of all as a presumed relictual species of ferns associated with
maximum is limited to that of the tree on which apparently relictual conifers as enclaves on some
they grow. Many fall in storms, often driven by heavily mineralised soils. One example is the oc-
their own weight, where they die and decompose currence of several Schizea species and the mono-
rapidly on the forest £oor, due to combinations of typic Stromatopteris moniliformis closely co-asso-
construction of many soft and semi-succulent ciating on ultrama¢c soils in New Caledonia
parts as a consequence of their growth rates. (Page, 2002a,b). The exploitation of the ability
By contrast, ultrama¢c sites clearly require un- to colonise a variety of low nutrient habitats is

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

a strategy which is probably widespread through (4^25 yr in packets, a maximum of 63 yr recorded

the fossil record for Pteridophyta, and doubtless on an herbarium sheet); and (3) the known resis-
has included, within its exponents, many di¡erent tance of fern spores to environmental hazards (see
groups of ferns. Many terrestrial ferns as far back Page, 1979b for an earlier review). These interpre-
as the Early Carboniferous have ‘sprawling’ or tations, however, equate closely with those de-
‘rampant’ habits (DiMichele and Phillips, 2002- rived by Cousens (e.g. Cousens et al., 1985, and
this issue) and one cannot help but note that personal communications 1980^1986), also based
this habit is characteristic of extant pteridophytes on independent experimental studies and parallel
surviving on the poorest edaphic terrains. ¢eld observations, which included the appearance
of taxonomically novel pteridophytes along the
3.5. High migrational ability of the airborne spore American Gulf Coast following episodes of hurri-
cane damage. I take a pragmatic approach and
The dispersal potential of the airborne pterido- simply begin from the practical stand-point that
phyte spore confers on ferns the potential of un- all fern spores have, and always have had, oppor-
usually high dispersal mobility. Main advantages tunity to get more-or-less everywhere given time.
arising from this appear to be: Sure, there will be a very rapid gradient of spore
(1) potential to continually arrive at sites of density dilution away from the parent plant.
poor access, such as rock-faces and, especially, However, spores can also disperse in long and
epiphytic sites; steady smoke-like plumes, and once airborne,
(2) potential to arrive rapidly at newly arising can enjoy great resistance to known environmen-
locations and thus pioneer habitats, such as land- tal hazards (see Section 3.6: Spore tolerance of
slide surfaces and new volcanic terrains; adverse aerial environments). I conclude that it
(3) potential to achieve (however occasional) is not dispersal per se that is usually limiting in
long-distance dispersal, from continents to ocean- terms of achievement of dispersal potentials in
ic islands or between remote island chains. pteridophytes (and that endless discussion of
These potentials are not mutually exclusive, and fern-spore migration abilities is a red-herring in
all possible combinations of one, two or all three terms of dispersal usually achieved). Instead, it
are clearly available. Furthermore, all are not is the opportunities for establishment of arriving
once-only events, but apply continuously to spore spores, against indigenous biotic competition, that
generation and release processes in most fern is the real issue determining and confronting eco-
communities. logical achievement and ultimate range: create the
All spore dispersal achievements are described appropriate habitat, and the appropriate pterido-
here as ‘potential’ since to what degree they are phyte coloniser will, sooner or later, appear there.
actually realised in nature is clearly complex and The likely e¡ect of distance is usually to in£uence
is yet only fragmentarily understood. Many var- the timing, rather than the actuality, of the event.
iations in circumstances must apply. Exactly how In this, disturbance regimes especially promote
signi¢cant long-distance dispersal might be in renewed colonisation opportunities, almost irre-
pteridophytes has, for example, long been a topic spective of where located, and biologically it is
of debate (e.g. Gregory, 1945; Lloyd, 1974a,b; probably those few spores that actually do get
Parris, 1985; R.M. Tryon, 1985, 1986; Kendall far that are the real ecological and evolutionary
et al., 1986; Lacey and McCartney, 1994; Caul- achievers.
ton et al., 1995; Schneller, 1996b), though there Some genetic evidence, which appears to sup-
are few exacting data on this issue. port these views, has been recently gained in the
My own interpretations are based on three lines case of the rare fern Dryopteris remota (Schneller
of evidence : (1) my personal ¢eld experience of et al., 1998). Furthermore, the activeness of many
fern £oras on oceanic islands in three major pteridophyte discharge mechanisms would appear
oceans today; (2) the known longevity of wide to have evolved particularly in response to selec-
taxonomic arrays of fern spores in captive storage tion pressures to optimise high mobility gain,

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rather than to fall near to the parent plant. Addi- Page, 1979b) still remains valid. This leads to the
tionally, as pointed out long-ago by Manton view that ferns spores are highly resistant to vir-
(1950), a single spore arriving by long-distance tually all of the conditions which they might be
dispersal must self fertilise if it is to establish a expected to meet during the course of airborne
¢rst colonising sporophyte. Most ferns appear to dispersal, even were this to be prolonged and at
have this potential (see Section 3.7: Flexibility of high altitude.
breeding systems to match varying ecological op- Additional aspects of spore viability-persistence
portunity). A genetic consequence of this is, of in the ¢eld in relation to soil spore banking have
course, that restoration of the diploid chromo- also recently been discovered in ferns (Dyer and
some number ensures that every gene becomes Lindsay, 1992, 1996; Lindsay et al., 1994).
homozygous and thus phenotypically expressed Schneller (1996b) has further shown an important
in the new sporophyte, irrespective of whether contribution by banked spores in helping to
that gene was recessive or dominant in the pre- achieve a potential, when exhumed, of forming
vious population. The haploid propagule thus en- many di¡erent genotypes at any location within
sures that long-distance originating founder pop- the population’s area. Furthermore, there is great
ulations can arise which are immediately di¡erent diversity in the architecture of fern spores (see, for
in detailed adaptation to those of their previous example, the many excellent illustrations of Tryon
population, and on which natural selection for and Tryon, 1982), yet almost nothing is known
that location at that time can consequently oper- about the adaptive and ecological signi¢cance of
ate. This would seem to be particularly signi¢cant their varying morphological characteristics. Some
both today and through geological time in the discussion of possible functional roles of spore
evolution of the fern £oras of remote sites, and ornamentation including in resistance and disper-
especially those of oceanic islands. sal, is given by Kramer (1977) ; A.F. Tryon (1986)
The dispersal facility conferred by the airborne and Van U¡elen (1986) and by Hemsley et al.
spore, creating an ever-present unseen ‘spore- (1999) ^ mainly on megaspores.
rain’, is clearly a powerful and constantly recur- Another result of extended spore viability is the
ring factor in pteridophyte ecology (Page, 1967a, ability conferred for migration and e¡ective long-
1986), and undoubtedly must have likewise have distance dispersal. The typically high proportions
been so virtually throughout the history of land of Pteridophyta in the £oras of oceanic islands
plants. In combination with some of the above (see Section 3.5: High migrational ability of the
tolerances, perhaps the most spectacular palaeo- airborne spore), demonstrate the e⁄cacy of this,
examples of the ‘spore-rain’ potential have been and may well have been one of the main selection
rapid achievement of ‘fern-spikes’ following the pressures for achievement of such viability poten-
great environmental disturbance events of the tials. Floristic patterns between such areas in the
Cretaceous^Tertiary and perhaps also the Trias- fossil record could well provide valuable indica-
sic^Jurassic boundaries (e.g. Spicer, 1989; Fowell tors of the progress of evolution of such achieve-
and Olsen, 1993; Srivastava, 1994; and see also ment. [A review of Mesozoic, Cainozoic and mod-
Collinson, 1996, 2002-this issue, for discussion). ern fern biogeography (Moran, 2001) will provide
a basis for future study of this topic.]
3.6. Spore tolerance of adverse aerial environments
3.7. Flexibility of breeding systems to match
Virtually all of the potentials outlined above varying ecological opportunity
would be negated if the fern spore was not viable
on arrival at a potential germination site. Long In addition to direct ecological achievements
distance dispersal may involve exposure to a shown by pteridophytes, relatively complex breed-
range of aerial extremes en route, including those ing systems exist which play important roles in
of extreme dryness, cold temperatures and irradi- endowing these plants with £exibility to con-
ation. Much of the earlier data on this topic (see stantly respond to environmental challenges. Three

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

mating-system patterns are generally recognised in Wagner and Wagner, 1985; Barrington, 1985;
ferns: sel¢ng (1) within or (2) between prothalli of Barrington et al., 1989; Page, 1990a,b, 1997b for
the same parent sporophyte (intragametophytic reviews).
and intergametophytic sel¢ng, respectively) and Thus, in addition to examples of ecological in-
(3) outcrossing between prothalli arising from £uences, we also need to look at breeding systems.
the spores of di¡erent parent sporophytes (inter- These genetic potentials have probably become
gametophytic crossing) (Klekowski, 1972a,b, increasingly varied and sophisticated through evo-
1973a,b, 1979, 1982; Soltis and Soltis, 1987, 1992). lutionary time. Nevertheless, many must be an-
While mating between prothalli, whether these cient in their basic origins and e¡ects, helping to
be from the same parent sporophyte or from dif- underpin a great diversity of fern ecological
ferent parent sporophytes, is clearly obligate in achievements throughout the fossil record. As
hetersporous ferns, in the majority of living ferns with phytochemical armament (see above), there
(which are homosporous) mating-systems are to a is much work yet needed in drawing comparisons
high degree £exible and opportunistic. The pro- between the breeding systems of more primitive
thalli of homosporous ferns have, in general, both and more advanced living taxa and setting this
male (antherdial) and female (archegonial) or- against the known fossil history and ecologies of
gans. There is normally a time-phase di¡erentia- the groups concerned.
tion between maturity of the organs of the two
sexes. However, there may also be a period of 3.8. Revivalist tendencies of certain gametophytes
overlap, and for most taxa, so far as is known,
either intragametophytic and intergametophytic In an experiment carried out by the author
sel¢ng can be an option only if out-fertilisation (Page, 1967b), prothalli of a range of mediterra-
by intergametophytic crossing fails. Outcrossing nean-climate ferns of the genera Notholaena and
is thus likely to be e¡ectively realised wherever Cheilanthes (Sinopteridaceae) (originating from
appropriate opportunity arises, and, with certain the Canary Islands) which were tested on an ex-
limitations (Schneller, 1996a), most ferns are ploratory basis, showed exceptional abilities to
widely regarded as being extreme outcrossers, withstand complete desiccation for enduring peri-
with only a few nearly exclusively inbreeders ods. Such desiccated prothalli were successfully
known (e.g. Ranker, 1992; Soltis and Soltis, 1992). rejuvenated from a ‘crisp and dry’ completely
Where whole populations of prothalli exist, air-dry state after storage for many months, by
then sexual balances amongst prothalli growing eventual return of overhead application of free
from homosporous spores are known to be fur- water, imitating rain.
ther mediated by antheridiogens (e.g. Schneller et Not all cellular sectors of each individual pro-
al., 1990; Korpelainen, 1997), the in£uence of thallus necessarily survived such treatment, but
which further encourages outcrossing and mini- enough green tissue persisted in most to act as
mises sel¢ng. In wild prothallial populations, the ‘revival centres’ from which new growth resumed,
e¡ects of such antheridiogens can be enhancement and from which complete new prothalli with new
of the reproductive success of small gametophytes sex organs then grew. Indeed, frequently more
through promotion of gender expressions, which than a single such centre persisted in single pro-
would not necessarily otherwise occur (Hamilton thallus, with the result that two or more new pro-
and Lloyd, 1991). The e¡ects of antheridiogens thalli resulted where there was formerly only one.
can operate between prothalli of di¡erent species Sexual maturity then followed, with the origin of
in establishment of contrasting sexuality. This is a completely new ‘replacement’ generation of
probably one of the factors promoting the num- sporophytes. This contrasted with the young spo-
ber of independent congeneric hybrids which rophytes of the same taxa arising from them,
have been ¢eld-recorded in pteridophytes (see which so far as my own observations have shown,
Rothmaler, 1944; Wagner, 1954; Walker, 1958; have no comparable desiccation recovery abilities.
Duckett and Page, 1975; Page and Barker, 1985; This glasshouse experiment con¢rmed earlier

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observations made independently on di¡erent spe- potentials of polyploidy). Main achievements of

cies by Pickett (1914). However, the existence of sporophyte longevity are:
this ability in ferns appears to have been little (1) capitalisation on success of achievement of
appreciated and I am not aware of any other the gametophyte stage and subsequent physical
studies that have been made since. The lack of retention of a hard-won niche;
extensive experiment across a broad taxonomic (2) that maximisation of sporophyte size can be
and habitat basis means that the extent of this achieved: this is important, for example, in gain-
ability of pteridophyte gametophytes is unknown. ing frond size exposure to most dispersive air-cur-
This is, however, a strategy in ferns which rent opportunities;
could have far-reaching potentials in opening cer- (3) spread of spore output of genetically suc-
tain habitats for a range of taxa today, and which cessful individuals over the longest number of
may well have been of signi¢cance in the past. years : this is of particular advantage, for example,
Prothalli could succeed under moisture regimes in achieving successful colonisation of habitats
which are intermittent and unpredictable, on a which appear only sporadically.
‘try and try again’ basis after an initial prothallial Assessments of longevity in fossil pteridophytes
foothold has been successfully gained. Such pat- in relation to past selection pressures in di¡erent
terns of survival could be advantageous in a num- environments would be valuable. However, it is
ber of di¡erent habitats, varying from sub-desert very di⁄cult to establish fern longevity in the fos-
sites to rock face habitats and even epiphytic sil record (Collinson, personal communication,
ones. In this behaviour, fern prothalli of a range 2001). One has to presume that tree ferns espe-
of genera are displaying a similar, if unexpected, cially must always have been long lived and that,
behaviour to mosses, suggesting that it could well amongst other Pteridophyta, horsetails must have
have relevance for the processes of fern-colonisa- been similarly so. Therefore, amongst the giant
tion even in apparently hostile conditions, both Carboniferous representatives of these plants
today and in the past. sporophyte longevity was probably the norm.

3.9. Potential longevity of resultant sporophytes 3.10. Exploitation of mycotrophy

An often overlooked advantaging strategy, Mycorrhizae have been widely recorded in as-
sporophyte longevity, may well be a particular sociation with the roots of extant ferns in ¢eld
feature of more ancient plants. It is also widely surveys in widely scattered locations (e.g. Burge¡,
present in extant conifers (Page, 2002a,b), and 1938; Cooper, 1976; Iqbal et al., 1981; Newmann
here too relatively especially so amongst many and Reddell, 1987; Jones and She⁄eld, 1988;
more ancient members. In ferns, examples of Gemma et al., 1992; Moteetee et al., 1996). This
sporophyte longevity include tree ferns from 150 suggests that such associations may well be a nor-
to 200 years (e.g. in cultivation at Penjerrick Gar- mal feature of the roots of the majority of extant
den in Cornwall) and Osmunda plants said to be ferns as well as ancient pteridophytes (Pirozynski,
up to 300 years old in cultivation. In the wild, the 1981, 1988; Taylor, 1990). As a generalisation,
rhizomatous fern Platyzoma is estimated to be there appears to be an emerging picture that my-
about 500 years old based on growth rates of 2^ cotrophy, though frequently present in the ¢eld
3 mm per year and the diameter of the ‘fairy ring’ gametophyte and sporophyte generations, is more
it had formed (Page, personal observations). obligate in more primitive (especially eusporan-
Drawbacks of vegetative longevity are perhaps giate) taxa (e.g. Montgomery, 1990), and prob-
that, in contrast to species with rapid life-cycle ably more facultative in most more advanced
turnovers, rates of adaptive change are committed (especially leptosporangiate) genera. This is sup-
to be slow. Slow life-cycle turnover may have con- ported by observations from experimental culture
tributed to evolutionary stasis seen in several pteri- which indicate that gametophytes of virtually all
dophyte groups (see Section 3.11: Exploitation of leptosporangiate taxa tested will grow successfully

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

aseptically, but there are other claims that ‘best’ produce plants of enhanced vigour, typically re-
growth is achieved when prothalli have access to £ected in increased size and/or faster vegetative
normal soil fungi (e.g. Hutchinson and Fahm, growth rates. Ferns have large numbers of small
1958). Where associations are facultative, it would chromosomes in cells with high cytoplasmic vol-
seem most likely that these could most advantage ume ratios. This enables many stages of chromo-
ferns either in terms of growth, perranation or in some doubling to be successively accommodated
achieving exploitation of unusual and perhaps ex- upon one another, while maintaining full opera-
acting ecological habitats, but remarkably little is tional integrity of the cells themselves during their
known about this. By complete contrast to ferns, crucial mitotic and meiotic divisional processes.
I know of no reports of mycotrophy in horsetails, Allopolyploid-derived tetraploids, octoploids and
though experiments I have carried out growing ploidy levels up to 16 ploid are known, and may
roots of Equisetum in aqueous culture (Page, be higher than this in some genera whose base
1967b) show that the sporophyte itself has long numbers are uncertain. Back-cross hybridisations,
and unusually persistent root hairs, which may between members of di¡erent ploidy levels within
well function in a similar manner. genera, appear to be just as common as crosses
Mycotrophy in pteridophytes is signi¢cant, between those of the same level. The permutations
however, in that it would appear to be of partic- which can result are many, progressively building
ularly ancient occurrence in primitive land plants complex reticulations of inter-speci¢c relation-
since at least the Early Devonian (e.g. Taylor, ships within individual genera (e.g. Wagner, 1954;
1990; Banks and Colthart, 1993). Data linking Hau£er and Windham, 1991; Hau£er et al., 1995;
between past pteridophyte diversity and exploita- Thomson, 2000).
tion of mycotrophy would be valuable, since such Additional outcomes in terms of fern genetic
relationships may well have provided a particu- potentials, which may be related to ploidy levels,
larly important advantaging strategy for fern suc- include the existence of hybrid swarms (¢rst pro-
cess in a wide array of habitats throughout geo- posed in Pteris by Walker (1958) and recently
logical time. con¢rmed by molecular work, for example in Po-
lystichum ^ Mullenniex et al. (1998). In addition
3.11. Exploitation of potentials of polyploidy there are multiple hybrids at the same ploidy lev-
el, some of which produce a percentage of appar-
The contribution which the exploitation of the ently good spores (Page, 1963, 1990a, 1997b). A
potentials of polyploidy (and especially allopoly- mechanism for stabilisation of hybrid reproduc-
ploidy) has made to the achievement of speciation tion at a homoploid level, autogamous allohomo-
in ferns has been one of the main areas of new ploidy, has also been proposed (Conant and
understanding in this group in the last 50 years Cooper-Driver, 1980). Opportunity also exists
(e.g. Manton, 1950; Shivas, 1961; Walker, 1958, for changes in mating systems, high genetic heter-
1966a,b, 1979, 1985; Page, 1967b, 1973, 1997a; ozygosity, the survival of genetic redundancy and
Lovis, 1977; Wagner and Wagner, 1980; Werth the ability for species, including narrow endemics,
et al., 1985; Soltis and Soltis, 1987; Barrington et to store high genetic variability (e.g. Chapman et
al., 1989; Hau£er, 1989a,b, 1992; Wolf et al., al., 1979; Gastony and Gottlieb, 1982). Also an
1990, 1991; Rabe and Hau£er, 1992; Hau£er et initially limited gene pool of an allopolyploid may
al., 1995). It has become clear that while autopo- be enriched as a result of multiple origins, muta-
lyploidy is only an occasionally successful evolu- tions and/or intergenomic recombinations (Werth,
tionary route in ferns, allopolyploidy is widely 1992). In established polyploids, silencing of du-
successful (Walker, 1979, 1985; Hau£er, 1996). plicate gene expressions (Werth and Windham,
Allopolyploidy allows for existing genomes to 1991; Gastony, 1991) and practical genetic dip-
be recombined in new and fertile taxa. It provides loidisation may subsequently ensue (e.g. Wolf et
a rapid route for species evolution and adaptation al., 1987, 1990). The whole process results in the
in ferns, and, where most successful, it tends to creation of morphological and ecological novelty,

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genetic diversity, maintenance of fertility, and ploidy stability and in part related to life-cycle
clear separation of genetic identity between dip- longevity, has been identi¢ed in several genera
loid progenitors and polyploid derivatives. The and species groups within the fossil record (e.g.
practical evolutionarily results are: Rothwell and Stockey, 1991; Delevoryas et al.,
(1) the speed with which new taxa of ferns can 1992; Rothwell, 1996a; Herendeen and Skog,
arise as pure-breeding lines; 1998; Phipps et al., 1998; McIver and Basinger,
(2) that resultant ‘instant’ taxa are each adapted 1989; Serbet and Rothwell, 1999; Pigg and Roth-
to somewhat di¡erent ecological conditions than well, 2001). High polyploids may be typical of
the parental taxa; and past activity in some ancient lineages, such as
(3) that such new taxa may combine new eco- Ophioglossum and Equisetum, while mechanisms
logical abilities with hybrid vigour. are also provided whereby opportunities for new
In consequence, in long-stable environments, it developments from old stocks (e.g. Page and
is likely that allopolyploids, though they may Barker, 1985; Ollgaard, 1992) can also rapidly
arise, will be seldom necessarily more successful occur.
than their parents if these are already ecologically
well-adapted. However, in more actively evolving 3.12. Biotic independence
£oras and under more changing environments,
higher ploidy derivatives can more often ¢nd Apart from mycorrhizal associations (see Sec-
niches clear for ecological success, probably even- tion 3.10: Exploitation of mycotrophy), and cer-
tually displacing many of the original ancestral tain known examples (e.g. the genera Lecanopte-
diploids. An extreme range of contrasts amongst ris, Solanopteris, Pteridium) where ferns gain
fern ploidy spectra is thus apparent. The long-sta- additional protection of their whole vegetative
ble and highly encapsulated fern £ora of the Can- structure by attracting ants (see Section 3.2: Di-
ary Islands has well under 30% polyploidy and verse phytochemical armament), there are few
these only of low ploidy grades (Page, 1967b, other pteridophyte^animal associations. The only
1973). This can be compared with the less con- ones of which I am aware, are the spiny spores in
¢ned and more actively evolving fern £oras of some Isoetes species (e.g. I. echinospora) which
either post-Pleistocene deglaciated areas of Eu- appear to be an adaptation to bird dispersal
rope (e.g. Manton, 1950; Vogel et al., 1998). or (Page, 1982b). Also some echinate spores, and
with what have been widely regarded as more the unusual lasoo-like ¢lamentous outgrowths of
modern tropical fern £oras (e.g. Jamaica and Tri- spore walls in Lecanopteris mirabilis, have been
nidad ^ Jermy and Walker, 1985; Walker, 1966a, suggested to be an adaptation to spore transport
1985). In these examples, over 70% polyploid rep- by the sporophyte’s associated ants (A.F. Tryon,
resentation, including high grades of ploidy, is 1985, 1986). It is, however, noteworthy that only
more typical. The former circumstances thus a very few known examples exist and a certain
have the greatest possibility of preserving relictual level of quite local evolutionary experiment seems
taxa in ferns (with many of the ferns of the Can- indicated, with methodologies which, in pterido-
ary Islands, for example, surviving today little phytes generally, appear not to have become
changed since the Miocene ^ Page, 1967b), the widespread.
latter for the success of much newer diversity. Throughout the vast bulk of pteridophyte di-
Even if only some of these aspects have applied versity, there appears to be remarkably little de-
throughout the past history of ferns the potential pendence on animals in general achievement of
conferred on ferns to meet new environmental the main life-cycle functions of vegetative growth,
challenges is clearly high. These mechanisms propagule dispersal or sexual achievement. Most
may well have contributed signi¢cantly and sub- ferns consequently constantly ‘shun’ rather than
stantially to fern ecological adaptive change and ‘court’ most animal species. This is in great con-
hence long-term fern survival and diversi¢cation. trast especially to the £owering plants, where
Evolutionary stasis, perhaps in part involving courting of animals (especially of pollinating in-

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

sects by £owers) has enabled often complex and 1938, 1954; Page, 1977, 1979a,b; Page and Clif-
sometimes bizarre pathways of achievement to ford, 1981; Johns, 1985), with over 12 000 species
evolve which are presumably more e¡ective than of ferns alone. In terms of species richness, homo-
could be achieved without such support. sporous pteridophytes are more successful than all
Two important advantages accrue, however, for other non-angiosperm grades combined (Roth-
ferns: well, 1996a). This account demonstrates that,
(1) Having established e¡ective pathways of amongst pteridophytes, similar general responses
biochemical defence mechanisms (see Section are shown time and time again by distantly re-
3.2: Diverse phytochemical armament), there is lated taxonomic groups in response to similar se-
an uncomplicating freedom to apply these without lection pressures. Using knowledge of the ecology
limitation throughout all the varied stages of the (especially autecology, life-cycle biology, environ-
plant life cycle. mental interrelationships and adaptations) of
(2) It has enabled the main life processes of ferns and fern allies today, an attempt is made
Pteridophyta, including dispersal and mating, to to analyse why pteridophytes are able to colonise
be achieved virtually exclusively with the presence such a range of habitats, and especially so many
of the simple physical agencies, which change lit- marginal ones. This synthesis is used to derive
tle with time. basic principles concerning the innate biological
Any partitioning of toxic e¡ects from certain weaknesses (limitations) and special strengths (ad-
organs or life-cycle stages is thus clearly unneces- vantages) of Pteridophyta as a whole, which are
sary if animals do not need to be courted. This presented here.
has contributed enormously to the fern’s freedom The seven limitations identi¢ed are innate
of specialisation in defence through the develop- weaknesses of pteridophytes, which clearly limit
ment of whole cocktails of diverse chemical fern potentials and achievements today. Clearly,
agents, against which animal groups are least none of these have been able to be successfully
likely to evolve complete defences. For example, ‘thrown-o¡’, to any major degree, in the course
in combination with other agents, the production of pteridophyte evolution. On this evidence, all
of insect ecdysones by ferns must be a defence to must have acted as similar limitations throughout
which it is di⁄cult for an insect to evolve resis- pteridophyte evolutionary history. Interestingly,
tance, even through geological time! few of these (perhaps only the single growing
Such biotic independence today almost cer- point (Section 2.2: Single growing-point limita-
tainly closely re£ects a life-style which probably tions of sporophyte architecture)) might be de-
began with the ¢rst vascular land colonisers. duced directly from the fossil record itself, and
Thereafter, through the dependence for dispersal most would therefore be unknown if we did not
and reproduction solely on only uncomplicated have evidence from the living plants.
physical agencies pteridophytes have audaciously, By direct contrast, the 12 advantages conserva-
solidly and unambiguously ‘pinned their colours’ tively identi¢ed (14 if including subcategories
to those agencies which neither change signi¢- within Section 3.2: Diverse phytochemical arma-
cantly through time, nor become extinct. Such in- ment, and Section 3.4: High tolerance of acute
dependence has contributed signi¢cantly to what nutrient disequilibrium substrates) clearly open
these plants have been able to achieve, and con- opportunity for exploitation of a considerable ar-
sequently to the close comparability between ray of ecological habitats by pteridophytes today.
modern and fossil pteridophyte life-styles. 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-
4. Discussion and conclusions binations, helping to explain the ecological diver-
sity which pteridophytes, and especially ferns,
Very considerable pteridophyte ecological di- have achieved. Experimental evidence indicates
versity survives today (Copeland, 1907; Holttum, that most of these advantages appear broadly

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C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33 23

across most taxonomic groups and seem to have is also targeted by the diverse phytochemical ar-
deep-rooted origins within Pteridophyta, to the mament of pteridophytes, which has a broad
degree that many are judged to be special innate spectrum of e¡ects on animals, especially against
abilities of these plants. On this evidence too, invertebrates. Uncontrolled high reproductive
most must have also been available to operate commitment, although doubtless a highly en-
throughout pteridophyte evolutionary history. ergy-intensive process, is combined with potential
Some, such as tolerance of extremes of edaphic longevity of resultant sporophytes. Together these
conditions, may have actually directly helped sur- attributes are e¡ectively exploited by the high mi-
vival of several ancient fern genera to occur grational ability ( = potential dispersal) of the air-
(Page, 2002d). Interestingly again, a few might borne spore, coupled with the known spore toler-
be proven, some others inferred, but many would ances to adverse environmental circumstances.
also remain unknown, especially in the potentials The breeding systems and their diversity are
which they liberate, if we did not have evidence clearly consequent on dispersal opportunities, no-
from the living plants. tably the facultative inbreeding fallback when
The 12 advantages help to mitigate, to tolerate, outbreeding fails which enables e¡ective long dis-
and sometimes to positively exploit, the worst ef- tance dispersal by a single spore. Today pterido-
fects of the seven limitations in a number of ways. phyta also gain ecological adaptation and evolu-
For example, the handicap of an independent ga- tionary advantage from their extensive
metophyte stage, the poorly controlled evapora- exploitation of potentials of polyploidy (especially
tive potential, and the need to ‘return to the water allopolyploid progression) and their high degree
to breed’ are all to a degree o¡set by the abilities of biotic independence. It is inferred that these
conferred by high disease resistance under satu- are also attributes with a long past history.
rated humidity levels. Upon this balance, low- Amongst living pteridophytes, ancient elements
light photosynthetic abilities then enable many as well as modern elements often co-exist (Stewart
such high-humidity but necessarily low-illumina- and Rothwell, 1993). Many fern families, notably
tion habitats, in which biotic competition levels Marattiaceae, Osmundaceae, Schizaeaceae, Glei-
are generally low, to become exploited to the cheniaceae, Matoniaceae, Dipteridaceae, Dick-
full. Slow plant growth rates may be less of a soniaceae, Cyatheaceae, Azollaceae, Salviniaceae
handicap under these often most stable of condi- and Marsileaceae, have well established, extensive
tions, while mycotrophic exploitation in gameto- fossil records (Collinson, 1992, 1996, 2002-this is-
phyte and sporophyte generations doubtless fur- sue ; DiMichele and Phillips, 2002-this issue ; Van
ther supports survival in these and many other Konijnenberg-van Cittert, 2002-this issue). Other
marginal habitats. Intolerance of widely £uctuat- non-fern pteridophytes, especially Equisetaceae
ing conditions by the sporophyte is, in appropri- (Page, 1972a,b), Selaginellaceae (Page, 1989) and
ate habitats, partly o¡set by the revivalist tenden- Lycopodiaceae (Wikstro«m et al., 1999) show evi-
cies of certain gametophytes. The single growing- dence of adaptive traits which must also have oc-
point limitations of sporophyte architecture are curred in the past biology, ecology and ancient
partly o¡set by many speci¢c morphological morphologies of these groups. Periods of evolu-
adaptations of genera. These are augmented fur- tionary stasis have been recognised, either from
ther by ecological escapism of many ferns to hab- the fossil record of single species such as those
itats which are either too remote (e.g. epiphytic) of Osmunda, Onoclea and Woodwardia (e.g. Roth-
or too toxic (e.g. heavily mineralised substrates) well and Stockey, 1991; Rothwell, 1996a; Phipps
for plant and animal pressures to be intense. et al., 1998; Serbet and Rothwell, 1999; Pigg and
These habitat opportunities are especially pro- Rothwell, 2001), or in whole pteridophyte £oras
moted by the unusual tolerance levels of ferns from their surviving cytology (Page, 1967b, 1973).
for sites of acute nutrient disequilibrium as well Similarly, there may be little change in at least
as the access to these regularly gained by the high some generic a⁄nities with habitats through
mobility of the airborne spore. Animal browsing time. Examples certainly include Onoclea, Osmun-

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

da and Woodwardia, which appear to have had sponsiveness, organisation and ecology have also
members associated closely with swamp habitat been emphasised within the Pteridophyta from a
margins similar to those of today since the Ter- fossil perspective since the Palaeozoic (DiMichele
tiary or earlier (e.g. Rothwell and Stockey, 1991; and Phillips, 2002-this issue), and a diversity of
Greenwood and Basinger, 1994; Pigg and Roth- habitats has been occupied through the Mesozoic
well, 2001; Collinson, 2002-this issue); Equisetum (Van Konijnenberg-van Cittert, 2002-this issue)
with similar habitats for at least as long (McIver and Cainozoic (Collinson, 2002-this issue). All
and Basinger, 1989) or very much longer (Page, of these alternatives will have operated, perhaps
1967b, 1972a); Acrostichum, characteristic today with varying emphases and in varying degrees,
of (uniquely) humid-tropical brackish-water es- between times of relative evolutionary quiescence
tuaries and swamps, and spreading into the sea- versus periods of more active radiation (Collin-
ward-face of mangrove swamps today, clearly as- son, 1991, 1996; Rothwell, 1987, 1999).
sociated with lakes and freshwater marshes in the Today their living survivors provide evidence of
Cainozoic (Collinson, 2002-this issue); free-£oat- the diversity of the innate mechanisms and pro-
ing water ferns (Azolla and Salvinia) in freshwater cesses which ferns are able to develop and exploit,
facies with a range of associated aquatic angio- and the diversity of adaptations and ecological
sperms widespread in the Cainozoic (Collinson, potentials which can thereby be achieved (Page,
2002-this issue); and gleicheniaceous and schi- 1997a, 2000, 2002c). These same innate mecha-
zaeaceous ferns as opportunists colonising open nisms and processes must have similarly occurred
and disturbed ground including ¢reburn sites throughout much of pteridophyte fossil history,
and volcanogenic terrains since at least Mid-Cre- opening similar ranges of adaptations and ecolog-
taceous (Collinson, 1996, 2002-this issue ; Van ical potentials, as strategic elements of recurring
Konijnenberg-van Cittert, 2002-this issue). More pteridological achievement.
contentious (Collinson, 2002-this issue) at present Although drawing comparisons between living
is the claim (Poole and Page, 2000) of a probable Pteridophyta and fossil ones is far from new,
Eocene epiphyte of Polypodiaceous a⁄nity, most such comparisons have been largely fossil-
though I maintain my conviction: if there are driven, and relate usually to speci¢c fossil taxa or
Polypodiaceae and there are trees, then there are habitats, seeking their modern equivalents for
epiphytes (though I do not dispute that additional comparison. Particularly important recent synthe-
evidence of these in physical connection would be ses have been made in this perspective by, for
valuable!). Fern epiphytes are proven in Palaeo- example, Rothwell (1987, 1991, 1996a,b, 1999).
zoic £oras, attached to tree fern trunks (Ro«ssler, The approach presented here is proposed as com-
2000; DiMichele and Phillips, 2002-this issue). plementary to that which can be gained from the
The ecology of living pteridophytes shows that fossils themselves. It is argued that the modern
this group is both complex and dynamic, and that fern ecologies help to point to a diversity which
these complexities still confer great versatility, could (and probably did) exist in Pteridophyta at
£exibility and adaptive e¡ectiveness, especially many times in the past. Using the same strategies
through their abilities of exploiting an unusually as their modern analogues, ancient ferns, at many
wide range of marginal habitat conditions. Ferns di¡erent times and locations, and with both sim-
have, in consequence, achieved long-term surviv- ilar and many di¡erent taxa to those of today,
al, diversi¢cation and success through evolution- have been similarly enabled to exploit a range of
ary time. Although primitive forms persist, diver- habitat miches as wide as those seen today.
si¢cation continues to occur on the basis of not
only modern stocks (e.g. Wagner, 1954; Hau£er
and Windham, 1991; Hau£er et al., 1995) but also Acknowledgements
on already ancient ones (e.g. Page and Barker,
1985; Page, 1972b, 1990a, 1997b; Ollgaard, On practical aspects, I am grateful for the
1992, 1996). Great evolutionary £exibility and re- support of several generations of horticultural

PALBO 2428 5-6-02

C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33 25

staff at the Royal Botanic Garden, Edinburgh, R.J. (Eds.), Pteridology in Perspective. Royal Botanic Gar-
dens, Kew, p. 651.
UK, for the day-to-day maintenance of my many
Axsmith, B.J., Krings, M., Taylor, T.N., 2000. A ¢lmy fern
pteridophyte and conifer experimental cultures for from the Upper Triassic of North Carolina. Am. J. Bot.
over more than 30 yr, and those at Oxford, UK, Abstr. Suppl. 87 (6), 66.
Brisbane, Australia, and Newcastle, UK, Univer- Balick, M., Furth, D.G., Cooper-Driver, G., 1978. Biochemi-
sities for extended periods before this. I am also cal and evolutionary aspects of arthropod predation on
grateful to the Royal Botanic Gardens, Kew and ferns. Oecologia (Berlin) 35, 55^89.
Banerjee, R.D., Sen, S.P., 1980. Antibiotic activity of pterido-
the Natural History Museum, London, for access phytes. Econ. Bot. 34, 284^298.
to herbarium materials, and to the Linnean Banks, H.P., Colthart, B.J., 1993. Plant^animal^fungal inter-
Society and Camborne School of Mines, Univer- actions in early Devonian trimerophytes from Gaspe Cana-
sity of Exeter, for access to library facilities in their da. Am. J. Bot. 80, 992^1001.
charge. On scientific aspects, discussions in the Barrington, D.S., 1985. Hybridisation in Costa Rican Polysti-
chum. Proc. R. Soc. Edinburgh 86B, 335^340.
laboratory, the field and the glasshouse, with Dr. Barrington, D.S., Hau£er, C.H., Werth, C.R., 1989. Hybridi-
Trevor Walker, Clive Jermy, Dr. Heather McHaf- zation, reticulation and species concepts in ferns. Am. Fern
fie, Dr. Adrian Dyer and Dr. Richard Bateman J. 79, 55^64.
have been long-term stimuli to the overall devel- Beck, A.L., Labandeira, C.C., 1998. Early Permian folivory on
a gigantopterid-dominated riparian £ora from north-central
opment and progress of these studies and to many
Texas. Palaeogeogr. Palaeoclimatol. Palaeoecol. 142, 139^
of the ideas contained therein. Dr. Heather 173.
McHaffie (Edinburgh, UK) has kindly provided Bernabe, N., Williams-Linera, G., Palacios-Rios, M., 1999.
additional pteridological comments and Dr. Mi- Tree ferns in the interior and at the edge of a Mexican cloud
chael Proctor (Exeter, UK) ecological comments forest remnant: spore germination and sporophyte survival
on the resulting manuscript. I am further grateful and establishment. Biotropica 31, 83^88.
Bohm, B.A., Tryon, R.M., 1967. Phenolic compounds in ferns.
to Dr. Margaret Collinson for her enthusiasm and Can. J. Bot. 45, 585^594.
support in helping to bring my neobotanical Bronstein, J.L., 1998. The contribution of ant^plant protection
concepts into a palaeo-botanic arena, and to her, studies to our understanding of mutualism. Biotropica 30,
Dr. Kathleen B. Pigg and Dr. Paul Kenrick for 150^161.
many helpful and constructive comments on the Brown, R.W., 1995. Bracken and the ecology of lyme disease.
In: Smith, R.T., Taylor, J.A. (Eds.), Bracken, An Environ-
resulting manuscript from a palaeo-botanic per- mental Issue, International Bracken Group, Aberystwyth,
spective. This paper is dedicated to the memory of pp. 116^119.
the late Professor Robert M. Lloyd (Athens, OH, Brousmiche, C., Coquel, R., Wagner, R.H., 1992. Late Stepha-
USA), the late Dr. Michael I. Coussens (Pensaco- nian Scolecopteris from the Puertollano Basin. Spain. Geo-
bios 25, 323^339.
la, FL, USA) and the late Professor Jan Kornas
Burge¡, H., 1938. Mycorrhiza. In: Verdoorn, F. (Ed.), Manual
(Krakow, Poland) all of whom contributed, in of Pteridophyta, Martinus Nijho¡, The Hague, pp. 159^191.
discussions and joint fieldwork, to the formation Cantrill, D.J., 1996. Fern thickets from the Cretaceous of
of some of the ideas included here. Alexander island, Antarctica, containing Alamatus bifurcatus
Douglas and Aculea acicularis sp. nov. Cretac. Res. 17, 169^
Castillo, U.F., Wilkins, A.L., Lauren, D.R., Smith, B.L., Tow-
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