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

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Ecological strategies in fern evolution:

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

Abstract

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
plants.
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.
PII: S 0 0 3 4 - 6 6 6 7 ( 0 1 ) 0 0 1 2 7 - 0

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

It is argued that collectively these weaknesses and strengths provide a broad framework, which, operating in varied
combinations, limit or open opportunities for exploitation of a considerable array of ecological habitats by
Pteridophyta. Based on these data, several general ecological principles are developed. It is proposed that, through
time, such strategies are likely to have opened many pteridophyte habitat opportunities, though not all of these will
necessarily have left directly identifiable signals in the fossil record.
Modern fern ecological limitations and advantages are shown to occur across broad taxonomic spectra and many
are innate abilities of the plants. It is, therefore, argued that a similar general 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-

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

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 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33 3

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

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

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

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

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6 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
able vulnerability is consequent should that grow-
ing point become damaged, and this basic archi-
tecture can also limit the £exibility of morpholog-
ical response (Gureyeva 2001). Additionally,
damage response, through development of new
lateral growing points as side-rhizome out-
growths, is usually slow. Main avoidance mecha-
nisms, which at least partly circumvent this innate
vulnerability, include:
(1) physical structure : this includes density of
hairs, scales and occasional spines to protect the
young expanding croziers ;
(2) removal of growing points to high above the
ground, such as in tree ferns: this avoids tram-
pling and direct foraging interest especially by
small- to medium-sized tetrapods;
(3) branching of the rhizomes : this provides
multiple rhizome-apex survival opportunities ;
(4) concentration of great species diversity in
sites of low browsing (and trampling) encounter :
¢de the great success of lithophytes and epiphytes
among ferns;
(5) high emphasis on biochemical armament ap-
parently e¡ective against a broad-spectrum of an-
imal taxa: see Section 3.2: Diverse phytochemical
armament.
In the case of tree ferns, particular vulnerability
then ensues from the creation of a trunk which is
itself a desirable habitat for colonisation by other
plants, notably by climbing epiphytes and scram-
bling lianes. All of these are harmful to tree ferns
since the inevitable upward growth of each is
drawn directly towards the single monopodial
tree fern crown. Further architectural develop-
ments by the tree fern are needed to counter these
advances. Two methods are adopted widely by
existing tree ferns. Some produce fast upward
growth resulting in a slender trunk which itself
has a smooth polished surface (with clean frond
abscission leaving only smooth leaf scars) upon
which it is di⁄cult for climbers to gain purchase.
Others, such as Dicksonia (Plate II, 1) and some
members of the Cyatheaceae and Blechnaceae,
have slow upward growth (resulting in a thicker
and more rough-surfaced root-clad trunk), but
they retain dense ‘skirts’ of old fronds hanging
below the crowns. These act as a foil to ascending
climbers and epiphytes which substantially fail to
PALBO 2428 5-6-02
negotiate round or through this ‘skirt’ (Page and
Brownsey, 1986).
Such crown vulnerability will have been char-
acteristic of ferns through the whole of the fossil
record, through which similar (and perhaps other)
strategic avoidance mechanisms will have been
elaborated. The presence of either exceptionally
clean trunks to fossil tree ferns or the presence
of persistent tree fern skirts would itself indicate
defensive mechanisms against the presence of
climbers or epiphytes in the associated palaeo-
£ora. It would seem that the Palaeozoic tree
fern Psaronius used neither of these deterrents ef-
fectively as it was colonised by both epiphytes and
climbers (Ro«ssler, 2000; DiMichele and Phillips,
2002-this issue) though these may have been re-
stricted to the lower part of the trunk.
2.3. Slow plant growth rates
Sporophyte (and sometimes gametophyte)
growth rates can vary widely between di¡erent
fern groups, speci¢c taxa, parents and allopoly-
ploid o¡spring (see Section 3.11: Exploitation of
potentials of polyploidy). They can also vary in
relation to location and habitat positioning within
the same species (e.g. Cousens, 1981). Neverthe-
less, in comparison with many angiosperms, over-
all fern growth rates are relatively slow (least so in
some epiphytes and some pioneer species), and
this has been suggested to be linked to the inher-
ently slow rates of some physiological processes in
ferns (Raven, 1977, 1984, 1985a). These include,
water movement in the xylem of purely tracheid-
based construction (Woodhouse and Nobel, 1982;
Gibson et al., 1985); di¡usive resistance (Wong
and Hew, 1976) and conductance of photosyn-
thetic carbon assimilation in mainly C3 pterido-
phytes, which are considered ‘‘generally towards
the low end of the range’’ for terrestrial tracheo-
phytes (Raven, 1985b).
Constraints imposed by growth rates in associ-
ation with the pteridophyte life-cycle (see Section
2.1: The handicap of an independent gameto-
phyte stage) also limit the capacity of pterido-
phytes to adopt short life-cycle turnovers of the
type which have enabled mosses as well as £ower-
ing plants to evolve small ephemeral forms (Ra-
 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
ven, 1985b; Richardson, 1992, p. 98). This is sup-
ported in conditions of experimental cultivation
where only a few exceptional examples have
been met which display rapid life-cycle turnovers
of the order of a year or less from spore-sowing to
sporophyte ¢rst spore production. These occur in
a few ‘modern’ genera (such as Anogramma and
Pityrogramma (both Gymnogrammaceae) and
Doodia (Blechnaceae)) and represent under 0.2%
of taxa personally cultivated in 40 years. Annuals
are thus rare in pteridophytes as a whole, and the
very great majority of ferns are thus committed
perennials, with inherently longer life-cycle turn-
overs (and often years to maturity) that this im-
plies.
Such multi-year perenniality seems likely to
have also been the case for most ferns in the
past. Furthermore, there is also a general trend
for greatest longevity to be achieved amongst sev-
eral taxonomically more ancient extant taxa (e.g.
Osmunda, Angiopteris, Equisetum), which may
mean that longevity may have been an even great-
er feature of even more pteridophytes in the fossil
record. That this is usually coupled to ultimate
size achieved should allow for appropriate fossil
signals to be identi¢ed and perhaps community
age-structure to be indicated, and might further
indicate palaeo-sites of adequate habitat stability
(see also Section 2.4: Intolerance of widely £uc-
tuating conditions). Occurrence of multi-aged
populations, including aged individuals, would
imply continuing habitat stability, and where re-
inforced by representation within the same com-
munity of high taxonomic and morphological di-
versity, would clearly indicate climax palaeo-
communities with multiple niche opportunities.
This seems to have been the case for some Palaeo-
zoic marattialean communities (DiMichele and
Phillips, 2002-this issue).
2.4. Intolerance of widely £uctuating conditions
Intolerance by unadapted sporophytes of
widely £uctuating conditions is a particularly
under-appreciated ecological limitation of the ma-
jority of ferns (Watt, 1976; Arens and Baracaldo,
2000). Fronds of most extant ferns (perhaps all),
appear to be able to make a once-only commit-
PALBO 2428 5-6-02
7
ment, such as on emerging, to habituation to am-
bient environmental conditions: light regimes,
moisture levels, air movement rates (Page, person-
al observations). Expanding fronds adapt to these
at the levels at which these environmental in£uen-
ces are met on initial frond expansion. Should
conditions subsequently change (such as increase
in light levels due to a tree fall gap forming in the
canopy) existing fronds appear unable to re-
adapt. Only subsequently emerging fronds adapt
as far as they are functionally able to the new
conditions encountered. Plants may require a
full growing season before all fronds borne be-
come modi¢ed to any major features of environ-
mental change. Furthermore, lack of stomatal
control, should conditions change, has been docu-
mented in Lycopodium species, with modest
amounts of inter-speci¢c variation (Heiser et al.,
1996).
Established sporophytes thus do not respond
well to environmental £uctuations, unless they
are ones to which a species is especially pre-
adapted. It is probably such inherent incapabil-
ities of short-term response that ensures that
fern sporophyte success is always greatest when
environmental conditions (of virtually all types)
remain most constant.
As a widely encountered example, it is almost
certainly for these reasons that, in temperate cli-
mates, fronds are delayed in emergence until the
tree canopy itself has mostly completed growth
(Page, 1988). Little would be achieved, and there
is everything to loose, by timing frond-expansion
to be any earlier than this. In tropical moist cli-
mates, however, where there is year-round forest
canopy shade-provision, new fern frond growth
can occur throughout the year. By contrast to
the single spring growth ‘£ush’ of fern frond
emergence of temperate regions, tropical fern
fronds arise typically in a steady and sequenced
year-round succession, accommodating ample op-
portunity for subsequent adaptation to any envi-
ronmental changes which do arise. Other varia-
tions occur in tropical dry climates, and in all
sites, further micro-habitat variations appear to
be involved. An interesting tropical example, The-
lypteris angustifolia, is being very closely docu-
mented by Sharpe (1996), in which seasonal rain-
8 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
fall patterns are closely re£ected in subsequent
development patterns of the plant. Such patterns
may well have considerable bioindicator value,
and need more detailed study.
If this fern preference for constant environment
also prevailed in the past, as seems likely, then
palaeo-environmental conditions can be inferred
from fossil fern £oras. For example, fern crowns
with fronds and frond buds simultaneously at
multiple stages of development (either on individ-
ual specimens or within populations) would be
usefully indicative of stability within a growing-
season (and could lead to an estimate of growth-
season length, such as in the wet tropics today).
By contrast, frond buds simultaneously at the
same stage would indicate growing-season release
within a more seasonally £uctuating environment.
A further signal reinforcing the latter, but in the
non-growing season, might be the additional pres-
ence of seasonally developed subterranean storage
organs. Root tubers on some ferns (e.g. Adian-
tum), if fossilised, would indicate dislodgement
during a dry-season interval. Equisetum, where
clearly fossilised with tubers, would indicate fos-
silisation in winter (between September and early
April in the northern hemisphere), and that the
aerial parts would have been deciduous and thus
not simultaneously present.
2.5. Poorly controlled evaporative potential
The general need for moist environments, with
low evaporative potentials to counter high rates
of water loss, characterises much of the life-cycle
of the majority of ferns (e.g. Wylie, 1948). This
problem places often severe limitations on the de-
gree of exposure which can be tolerated by many
ferns. Such poor control clearly restricts pterido-
phyte and especially fern success on both a re-
gional and a habitat basis, and is certainly also
highly taxon-speci¢c. It is a noteworthy aspect of
this limitation in living fern taxa, that individual
species are often limited by particular levels of
soil-water availability, as well as surrounding air
humidity. Furthermore, even within the same
habitat, di¡erent species can have subtly di¡ering
requirements, including lateral movement and
particular aeration levels of the soil water present.
PALBO 2428 5-6-02
In Equisetum, Equisetum £uviatile tolerates the
most anaerobic (and still) water conditions, while
at the other extreme, Equisetum telmateia requires
the most oxygenated water, and is indicative of
constantly moving water sites (such as especially
that below springlines Page, 1988, 1997b). Such
aspects of micro-habitat di¡erences must also ap-
ply to many pteridophytes in other sites.
Climatic factors especially closely in£uence
pteridophyte success and di¡erentiate closely be-
tween that of di¡erent fern species. These include,
in particular, such factors as frequency of precip-
itation and its temporal distribution (i.e. not just
overall amount), degree of exposure versus shel-
ter, and factors linked more indirectly to evapo-
ration such as cloud-cover. There is, as yet, re-
markably little accessible data on most of these
aspects even for living pteridophytes. It requires
diligent e¡orts to draw such information together
even for well documented areas such as Britain
and Ireland (see, for example, maps of several
factors especially signi¢cant to pteridophytes gen-
erated on long-term accumulated data by the Brit-
ish Meteorological O⁄ce in Page, 1982b).
There is considerable potential to exploit pter-
idophytes as discriminating and sensitive environ-
mental indicators, both for the present and the
past, using approaches being more widely devel-
oped (and funded!) mainly by agro-meteorologi-
cal and forestry sources (see especially Thompson
et al., 2000). Fern £oras and nearest living rela-
tives (‘indicator species’) could both be applied in
palaeo-environmental studies. Environmental in-
dicators could be used, for example, for establish-
ing relative comparisons between habitats and
niches in separated palaeo-locations (cf. the mod-
ern Equisetum example cited above).
2.6. Uncontrolled high reproductive commitment
Nearly all pteridophyte sporophytes, including
ferns of most genera, have a high and largely un-
controlled annual reproductive commitment.
Once an appropriate stage of maturity for an in-
dividual sporophyte has been reached, spores are
typically produced in prodigious numbers
throughout the remaining life of the plant. This
may be over decades or more (Gureyeva 2001).
 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
As a consequence of this production rate, extra-
ordinary levels of over-saturation must regularly
occur in terms of what is necessary to maintain
individual populations within existing commun-
ities, where the great majority of spores must in-
evitably fall (e.g. Conant, 1978; Dyer and Lind-
say, 1992; Bernabe et al., 1999). The price of such
over production, and the inability of most ferns to
control it, must be a considerable drain on recur-
rent energy commitments by the parent sporo-
phyte. These levels of commitment, the apparently
highly sacri¢cial nature of much of the process,
and the fortuitous roles of chance are probably
little di¡erent in character today from those which
typi¢ed the life histories of ferns through their
long palaeo-history.
This disadvantage is, however, a two-edged
sword, since some clear advantages may well also
be gained by large spore numbers. These are dis-
cussed in Section 3.5: High migrational ability of
the airborne spore. Of these, signi¢cant in a pa-
laeo-perspective are likely to be combinations of
recurrent arrival at sites of poor access, abilities of
potentially long-distance dispersal, and of rapid
exploitation of sites immediately following post-
disaster scenarios. All, and especially the latter,
open opportunities for serial successions to begin
to involve pteridophyte sporophytes from the ear-
liest stages, in potentially large numbers. These
have, through the fossil record, doubtless greatly
in£uenced the overall ability of pteridophytes
(and especially ferns) to become exploiters of the
epiphytic niche. However, this may seldom be a
habitat of high preservation potential (Poole and
Page, 2000) and is hard to document in the past
(DiMichele and Phillips, 2002-this issue).
2.7. Need to ‘return to the water to breed’
The need for the existence of free water, even if
only as a ¢lm, is essential for sexual fertilisation
by free-swimming motile antherozoids within the
immediate habitat niche in which the prothalli of
the gametophyte generation actually grow. Apart
from in the example of occasional apomictic ga-
metophytes (see Section 3.7: Flexibility of breed-
ing systems to match varying ecological opportu-
nity), reproduction for most pteridophyte species
PALBO 2428 5-6-02
9
is thus limited to occasions and locations when
such free water exists. Observations in experimen-
tal culture (Page and Walker, independent person-
al observations) show that for some species this
may be as ¢nely tuned as speci¢cally timed an-
therozoid release (and perhaps archegonial recep-
tivity) over only certain periods in seasonal and
even diurnal cycles, with which such free water
has to necessarily coincide. This is a little-appre-
ciated factor which may well contribute substan-
tially to detailed delimitation of pteridophyte
niches, habitats and overall ranges, as well as hy-
brid occurrence (and thereby evolutionary success
(see Section 3.11: Exploitation of potentials of
polyploidy).
In this respect, the Pteridophyta as a whole are
very much the plant Kingdom’s equivalent of the
Amphibia, between which there are many broad
similarities in ecology, life-style, tropical diversity,
habitat range, moisture limitations and the con-
tinuing occurrence of a free-living ‘juvenile’ phase
(Page, 1985). Such similarities and limitations
must have applied at least equally strongly
throughout the pteridophyte fossil record, where
other pteridophyte^amphibian analogues might
also exist.
Clearly, for almost all pteridophytes, the achilles
heel of a free-water requirement will have been
experienced throughout their past history, to the
degree that fossil pteridophyte presence is neces-
sarily indicative of the presence usually moist en-
vironments, in which adequate free-water (chie£y
by precipitation) will at some time have been
present. To a large extent, pteridophyte taxonom-
ic and morphological diversity today is a measure
of the regularity and reliability of occurrence of
such water ^ ¢de the overwhelming abundance
which ferns can achieve in the regularly moist
cloud zones of tropical mountain mist forests to-
day. (This limitation clearly links closely to that
of Section 2.4: Intolerance of widely £uctuating
conditions, and Section 2.5: Poorly controlled
evaporative potential, and also to Section 3.3:
High disease resistance under saturated humidity
levels). Sites of exceptional fern diversity within
the fossil record, coupled with analysis of the eda-
phic niches occupied by the species and life-forms
involved, can potentially provide a valuable tool
10 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
towards determining aspects of water availability
in various palaeo-environments.
3. The recurring advantaging strategies of fern
ecology, adaptation and survival
In contrast to the seven limitations above, the
advantaging strategies of fern ecology (12 are
identi¢ed here as 3.1^3.12) are the ‘positive’ side
of fern potentials, adaptation and survival. These
compliment those of the ecological approach of
Grime (1977, 1985). These strategies re£ect recur-
ring pteridophyte strengths today and are likely to
have done the same throughout the history of
pteridophytes.
In deriving an analysis of these strategies, the
extant ferns provide a resource-rich information
base, in which laboratory work and experimental
cultivation each contribute a substantial experi-
mental database. The evidence is combined here
with information from the ¢eld to achieve an
overall broad ecological synthesis. The evidence
supports the view that many clear and de¢nable
principles of survival exist amongst extant fern
taxa, governed by innate abilities of the plants
themselves, and which occur across broad taxo-
nomic spectra.
3.1. Low-light photosynthetic ability
Virtually all observational fern ecology today
would support the view that many ferns survive
particularly well in levels of light which are too
low for most competing angiosperms (as well as
many conifers) to tolerate, but I am aware of few
exacting physiological measurements which ad-
equately quantify this. Complete photosynthetic
saturation at low levels of incident light would
appear to be the key factor (Page, 1979b). Arina-
wati et al. (1996), for example, quote high total
chlorophyll levels and particularly low light-satu-
ration photosynthetic rates of fronds of the trop-
ical climber Teratophyllum rotundifoliatum (which
has fronds in both low and high light levels), and
indicate that di¡ering in£uences of light type may
also be involved.
Fern species of low-light habitats (which are
PALBO 2428 5-6-02
very many, e.g. Plate II, 3) exploit a niche in
which competition pressure today is substantially
reduced. These abilities undoubtedly greatly facil-
itate the occupation of a wide range of niches in
forests, from deep shaded ravines to dark forest
£oors, as trunk epiphytes and climbers, and as
plants of highly cloudy or frequently misty envi-
ronments. Low light-saturation e⁄ciencies will
have been a particularly important factor through
the course of angiosperm radiation (e.g. Crane,
1987). Such shade-tolerating potentials have al-
most certainly been available to ferns in habitats
of earlier forest types too (e.g. Thomas, 1985) and
could well have evolved, for example, as adapta-
tions to highly cloudy and misty environments,
very long before angiosperm diversi¢cation.
Probable forest-£oor shade tolerant taxa (on
the basis of their nearest living relatives) are
known in some palaeo-£oras (e.g. Rothwell et
al., 1994; Stockey et al., 1999). Large and delicate
fern fronds are also represented in the fossil rec-
ord (e.g. Deng, 2002-this issue) and so are ferns of
the shaded woody habitats of peat-forming
swamps (Collinson, 2002-this issue; DiMichele
and Phillips, 2002-this issue; Van Konijnenberg-
van Cittert, 2002-this issue). However, ferns of
shade habitats are, from evidence of living species,
frequently soft and/or thin-fronded and of gener-
ally delicate texture. Plants of such structure (es-
pecially extremes like Hymenophyllaceae) would
seem to o¡er a particularly low potential to nor-
mally become well-represented (at least as macro-
fossils) in most fossil £oras. By contrast, the
coarser-textured often higher biomass, tough
structures (especially stipes) and frequently more
monospeci¢c counterparts (e.g. Plate I) of more
open habitats have higher fossilisation potential
(e.g. Collinson and Ribbins, 1977; Yao and Tay-
lor, 1988; Skog, 1992; Rees, 1993; Gandolfo et
al., 1995; Cantrill, 1996). (Today, these ferns in-
clude genera such as Dennstaedtia, Lonchitis, His-
tiopteris, Hypolepis, Paesia, Pteridium.) This ta-
phonomic bias should be taken into account
when interpreting fern £oras of the past.
3.2. Diverse phytochemical armament
Mostly only becoming known in the last 25 yr,
 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
diverse phytochemical armament is probably the
most e¡ective and widespread strategy in promot-
ing direct vegetative survival of Pteridophyta as a
whole. It is becoming clear that phytochemical
armament, of widely di¡ering degrees and types,
is taxonomically widespread in ferns and other
pteridophytes, and appears to be the prime anti-
herbivore grazing defence mechanism of both gen-
erations.
Such biochemical armament has clearly become
an e¡ective route of defence for such a predom-
inantly herbaceous group with relatively slow
growth rates (see Section 2.3: Slow plant growth
rates), vulnerable growing points and organs and
lack of most other physical defences or herbivore
avoidance mechanisms (see Section 2.2: Single
growing-point limitations of sporophyte architec-
ture). It probably also contributes substantially to
the survival of gametophytes, and thus to mitigat-
ing against the apparent vulnerability of this free-
living stage (see Section 2.1: The handicap of an
independent gametophyte stage). Such biochemi-
cal armament, however, undoubtedly requires
continuing resource and energy commitments on
the part of the plant, but it avoids the need for
development of elaborate physical defence struc-
tures, thus enabling relatively simple pteridophyte
architectural form to persist.
Nevertheless, remarkably little is yet under-
stood about which of any known phytochemical
substances are employed to achieve e¡ective de-
fence and exactly what they are targeted against.
Currently we are only aware that present targets
seem broad, and were probably similarly so in the
past. Field botanists will be aware, however, that
few modern ferns usually show signs of any sig-
ni¢cant herbivory in the ¢eld. Even to a human
nose, many ferns have distinctive (and often spe-
cies-speci¢c) odours (e.g. Plate II, 2), some of
which are quite curious: e.g. the temperate Gym-
nocarpium robertianum (Athyriaceae) which has
an apple-like fragrance, Polypodium glycyrrhiza
(Polypodiaceae) which smells of liquorice, and
the tropical Anemia phyllitidis (Schizaeceae) which
smells to me of running model railways !). The
research which is available suggests that, in most
ferns, general browser interest appears to be suc-
cessfully checked (or at least, held to a minimum)
PALBO 2428 5-6-02
11
by cocktails of biochemical repellent pathways in-
volving sometimes complex chemical components
(Bohm and Tryon, 1967; Hayashi et al., 1977;
Cooper-Driver, 1978, 1985; Balick et al., 1978;
Jones and Firn, 1978, 1979; Gerson, 1979; Had-
¢eld and Dyer, 1986; Suksamrarn et al., 1986;
Smith et al., 1990).
Sporophytes of Bracken (Pteridium) have been
more extensively studied in this respect than any
other fern, and provide a valuable generic exam-
ple. Pteridium is known to contain a particularly
formidable armoury of repellents, from tannins
and sesquiterpenoids to phenols and cyanide (as
a cyanogenic glycoside), plus two carcinogens, a
leukaemiagen and, for good measure, a broad-
spectrum insect ecdysone. Collectively, or sepa-
rately, these can have dire e¡ects on potentially
browsing animals of many types (e.g. Harding,
1972; Cooper-Driver and Swain, 1976; Evans,
1976, 1986; Hendrix, 1977; Temple, 1981;
Schreiner et al., 1984; Fenwick, 1988; Had¢eld
and Dyer, 1988; Saito et al., 1989; Galpin et al.,
1990; Low and Thomson, 1990; Smith et al.,
1990; Wells and McNally, 1995; Bronstein,
1998; Thomson, 2000). Allelopathic compounds,
toxic to other plant growth, are also copiously
produced by bracken (e.g. Gliessman, 1976;
Gliessman and Muller, 1972) and probably by
many (? most) ferns (Weinberg and Voeller,
1969; Banerjee and Sen, 1980). Furthermore, at
least in Pteridium, the spores also are known to be
substantially armed with some of the same com-
pounds in even higher concentration per dry
weight than in the vegetative body of the plant
(Evans and Galpin, 1990). These compounds are
presumably e¡ective against sporophagy during
both pre-dispersal and post-dispersal phases.
Fern fronds can and do, however, provide
roosting-habitats for a great number of terrestrial
arthropods (e.g. Lawton, 1976; Gerson, 1979; Ot-
toson and Anderson, 1983; Lawton and MacGar-
vin, 1985; Brown, 1995; Jensen and Holman,
2000) with which the plants appear to successfully
co-exist. A limited tolerance to a degree of grazing
appears to exist between ferns and some insects,
notably Lepidoptera and sometimes Hemiptera
(Balick et al., 1978; Lawton, 1982; Lawton and
MacGarvin, 1985; Weintraub et al., 1995). Addi-
12 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
tionally, various ant^fern associations and mutu-
alisms are becoming recognised (e.g. Darwin,
1877; Southwood, 1977; Page, 1982a; Lawton
and Heads, 1984; A.F. Tryon, 1985; Walker,
1985; Arens and Smith, 1998). Sometimes further
defensive bene¢ts to the plant may be gained by
tolerating the presence of such animals, and some
defence mechanisms, expensive in energy invest-
ment, may be discontinued when not needed.
An example of this is in the specialist myrmeco-
philous epiphytic Lecanopteris carnosa (Polypo-
diaceae). Experience in glasshouse cultivation
(Page and Walker, personal observations, 1964^
1967) shows that this species has prothalli and
young sporophytes which are especially attractive
to rapid and usually terminal depredation by
small slugs. However, in the wild, this species is
regularly and aggressively ant-colonised (and is
here inferred to be likely to be mutualistically
ant-protected) on the branches of the tropical
lowland swamp-margin trees on which these large
epiphytes normally grow (Jermy and Walker,
1975). It is presumed here that chemical defences
have been dropped when other alternative (less
energy-consuming) defence mechanisms have be-
come available. Our observations showed that the
same slugs and snails did not similarly attack a
broad range of other adjacent fern cultures. This
provides at least some negative evidence of a nor-
mal defence in most pteridphytes (presumably
chemically mediated) which would appear to be
sensed, and thus avoided, by slugs, snails and pre-
sumably other invertebrates.
Some of the e¡ects of pteridophyte chemical
constituents today are responses to potential mi-
crobial attack (e.g. Kobayashi et al., 1975; Baner-
jee and Sen, 1980). However, it is mainly against
browsing pressures, especially by arthropods (e.g.
Wootton, 1981, 1990; Scott et al., 1985, 1992,
1996) that selection pressures for the development
of such a diverse array of phytochemical arma-
ment (and a diversity of arthropod counter-mea-
sures) will have been recurrently stimulated. Very
few other ferns have been studied in any compa-
rable detail to Pteridium, although the list of taxa
and known phytochemical isolates and their di-
versity of e¡ects on modern browsing animal
groups is steadily growing. The extent of these
PALBO 2428 5-6-02
indicates a high probability that such defences
are general in most living pteridophytes. They
can be varied (e.g. through a number of di¡erent
secondary compounds focussing especially,
though not exclusively, on a diverse range of cy-
clopropane compounds ^ Potter, 2000) and pro-
mote, amongst other e¡ects, onset of degenerative
conditions in a broad spectrum of animals expe-
riencing them. Other contained compounds, such
as ecdysones, are more arthropod-speci¢c.
Also essentially phytochemical in origin (and
almost worthy of a separate entry as a further
independent advantaging attribute of ferns, were
there clearer evidence), is the occurrence in ferns
of chemically unusual intra-cellular cements,
which bind cells together (Manton, 1950). As far
as I am aware, in contrast to all phytochemically
toxic aspects of ferns, nothing is known about
these, beyond that they contrast with those of
all £owering plants. In ferns, these have the repute
of not being soluble in hydrochloric acid, and of
hence making fern frond material indigestible to
all animals dependent on an HCl-mediated diges-
tive system. Indeed, slugs and snails are the only
animals known (at least by repute amongst pter-
idologists) to have the necessary stomach enzymes
with which to attack these fern cements. I person-
ally regard this as a potentially important survival
strategy in ferns (and possibly in other pterido-
phytes) against animal depredation, but, so far
as I am aware, the whole topic appears virtually
unresearched. It could, however, have consider-
able implications both for the survival of ferns
against a range of herbivores through time. Fur-
thermore (especially if it also operated against de-
cay organisms ^ I do not have any evidence either
way), it may also have a¡ected the preservation
potential of ferns throughout the fossil record.
Pteridophytes as a whole have been the focus of
general browsing attention (including detritivory)
especially from invertebrates (such as Oribatid
mites ^ Labandeira et al., 1997) since the Carbon-
iferous or earlier (e.g. Scott and Taylor, 1983;
Jeram et al., 1990; Stephenson and Scott, 1992;
Scott et al., 1985, 1992, 1996; Jarzembowski,
1994; Collinson, 1996; Labandeira and Phillips,
1996; Labandeira, 1998). There are some indica-
tions, from Palaeozoic compression £oras, that
 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
fern leaves were already then less browsed than
alternative vegetation (e.g. Beck and Labandeira,
1998; Collinson, 1996, p. 380^381) and, although
the Palaeozoic tree fern Psaronius exhibits a host
of arthropod interactions these do not seem to
include leaf-feeding (Labandeira, 2001). During
this long period of interaction, evolutionary pres-
sures for the development of adequate armament
must have been intense, constant and diverse in
most habitats in which Pteridophyta have suc-
ceeded. Clearly modern ferns enjoy considerable
abilities to achieve complex biochemical defence
potentials (e.g. Hartzell, 1947; Evans and Mason,
1965; Hayashi et al., 1977; Swain and Cooper-
Driver, 1981; Ojika et al., 1987; Saito et al.,
1989; Kushida et al., 1994; Castillo et al., 1997;
Potter, 2000; Siman et al., 1995, 2000). Doubtless
many other variations have occurred through the
fossil record against the same selection pressures.
Increasingly, evidence is that the pathways of
known defence involved are, chemically speaking,
complex; biologically speaking, e¡ective; and
evolutionarily speaking, diverse and often subtle.
The main measure of the speci¢c e⁄cacy of bio-
chemical defences through the fossil record is
most likely to be gained through assessments of
actual recordable incidences (and hence inferred
susceptibility) of browsing activity (foliar/spore)
between contemporaneous taxa and through
time (like that of Wilf and Labandeira (1999)
for angiosperms). Unfortunately, for the fossil
record, those taxa which were highly susceptible
will be those least likely to be represented. How-
ever, clearly the Pteridophyta are not mere begin-
ners at these diverse and extensively practised
achievements!
3.3. High disease resistance under saturated
humidity levels
Once past the life-cycle hurdles of spore surviv-
al (including possible survival as soil spore-banks
^ see Dyer and Lindsay, 1992), potential sporoph-
agy (e.g. Leschen and Lawrence, 1991) and
achievement of successful germination and estab-
lishment (see Weinberg and Voeller, 1969; Dyer,
1979; Lloyd and Klekowski, 1970; She⁄eld, 1996
for reviews), ferns succeed under humidity re-
PALBO 2428 5-6-02
13
gimes within which most £owering plant seedlings
would readily ‘damp-o¡’ through rapid fungal at-
tack. Cultivation experience shows that intrinsic
pathogen resistance abilities are taxonomically es-
pecially widespread in ferns and are expressed ef-
fectively in both the gametophyte and the sporo-
phyte stage to the great competitive ecological
advantage of the fern. Extreme examples must
be the ¢lmy ferns (Hymenophyllaceae), many of
whose members grow permanently and success-
fully in habitats such as the spray-zones of trop-
ical waterfalls, where the £imsiness of the fronds
(Plate II, 4) might appear to scarcely make a side-
salad for a self-respecting pathogen! The mecha-
nisms of such tolerance are very little understood,
though antibiotic e¡ects have been reported in
ferns (e.g. Kobayashi et al., 1975; Banerjee and
Sen, 1980).
Thin-fronded ‘¢lmy ferns’ (which have been as-
signed to the Hymenophyllaceae) are known from
the Mesozoic (Deng, 1997; Axsmith et al., 2000)
implying a long history for ferns growing in satu-
rated humidity levels. Signi¢cantly, many of the
ferns in a diversity of distantly related families in
this habitat today are successfully bulbiferous,
often developing a ‘walking-fern’ habit and/or de-
velop axillary branching patterns of growth. Such
habits occur in few other habitats, and hence
would provide an important marker in the fossil
record for such humidity and moisture regimes.
3.4. High tolerance of acute nutrient disequilibrium
substrates
Two suites of factors here (which could almost
rank as separate advantaging strategies in their
own right) operate either independently or collec-
tively in achieving unusually high and varied nu-
trient disequilibrium tolerance amongst modern
ferns.
These suites are: (1) a direct ability to tolerate a
range of exceptionally low nutrient terrains (e.g.
Plate II, 5); (2) an additional ability to tolerate
additional unusual levels of excess mineral ele-
ments which can also be present in some of these
terrains, and which can be at levels that would be
toxic to many other plants (e.g. Plate II, 6).
Field ecology suggests that these tolerances ap-
14 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
pear to be possessed, either separately or collec-
tively, within an especially wide taxonomic array
of genera and families of extant ferns (e.g. Con-
way and Stephens, 1957; Kruckeberg, 1964, 1976,
1964, 1976, 1984; Holbrook-Walker and Lloyd,
1973; Lloyd, 1976; Kornas, 1978, 1985; Page,
1979b, 1988, 1999; Sleep, 1985; Spicer et al.,
1985; Malaisse et al., 1994; Tsuyuzaki, 1997).
Within each suite, wide and diverse spectra of
actual tolerance levels and types doubtless exist.
In the second suite, wide variations in the individ-
ual minerals which can be tolerated almost cer-
tainly exist, although beyond ¢eld observations,
there is yet little available quanti¢ed data on
this. Amongst the ¢rst suite, subtle di¡erences
amongst tolerances of epiphytic taxa are re£ected
in the tendency (in the tropics especially) for dif-
ferent pteridophyte epiphytes either to be general-
ist or more narrowly specialist species as far as
preferred host-tree habitat selection is concerned
(cf. Gardette, 1996). Signi¢cantly, in both suites,
species with di¡erent apparent substrate preferen-
ces (presumed a re£ection of di¡erent tolerances)
frequently occur within the same genus. This sug-
gests that the detailed tolerances have evolved
very numerous times in ferns, adapting individual
taxa closely and subtlety to e¡ective exploitation
of particular local habitat opportunities.
There are strong contrasts between the ability
to succeed in the ¢eld on generalised, open, but
strongly limited terrains versus (at the extreme
opposite) within exuberant mature mesic forest
vegetation. These contrasts emphasise the roles
of physical/chemical versus biotic pressures with
which respective pteridophytes are confronted.
Mature forest vegetation, and especially rain-
forest, is widely appreciated to be a very complex
community, within which niche preferences be-
tween fern species are almost certainly very pre-
cisely and exactingly di¡erentiated (e.g. Page,
1979b, 1988; Petersen, 1985; Cousens et al.,
1988; Young and Leon, 1989; Van der Wer¡,
1992; Tuomisto and Ruokolainen, 1994; Poulsen
and Neilsen, 1995; Poulsen and Tuomisto, 1996;
Tuomisto and Poulsen, 1996). Most pteridophyte
species from such sources can be successfully
reared in glasshouse culture (personal observa-
tions 1958^2001) on relatively arbitrary standard-
PALBO 2428 5-6-02
ised horticultural compost media (including,
ironically, most epiphytes, providing that they
are not over-fed with standard nutrient additives).
This indicates that the often high localisation of
forest species in the ¢eld is not purely (or even
mainly) the result of narrow mineral tolerances
and speci¢cities (beyond the general one of epi-
phytes). Instead, the niche-width of these in the
wild (often extremely narrow, sometimes also
highly localised) is mainly prescribed by overrid-
ing interactions of immeasurably subtle, complex,
and highly pervasive, biotic competition.
By contrast, ability to succeed on more gener-
alised terrains with lowered (or initially virtually
zero) biotic competition can open wide habitat
opportunity for those species which are able to
achieve high tolerance levels of the ruling nutrient
disequilibriums. For these, the edaphic speci¢city
can seem very high. Yet many pteridophytes
which are vigorous (sometimes to the extent of
being rampant) in edaphically low-nutrient habi-
tats in the wild (notably, for example, many Ly-
copodiaceae, virtually the whole of the Gleiche-
niaceae and Lindsaceae, Dipteridaceae, Matonia
and Christensenia, and most Schizaeaceae) can,
ironically, prove extraordinarily di⁄cult to grow
at all in conditions of experimental cultivation !
Extremely high and exacting directly edaphically
limited tolerances and limitations seem indicated
for such pteridophytes.
Both suites of this nutrient disequilibrium tol-
erance strategy, either separately or in combina-
tion, advantage ferns in enabling them to grow in
a wide range of sites which are either too nutrient-
poor or are too high and toxic in unusual (e.g.
metalliferous) elements for most other competi-
tors to succeed equally well. The net e¡ect of
these abilities is to open a variety of low-competi-
tion habitat opportunities for colonisation into
sites which can be widely available to pterido-
phytes because of the migratory e⁄ciency of the
airborne spore (see Section 3.5: High migrational
ability of the airborne spore). Typical habitat ex-
amples include:
b intrinsically nutrient poor sandy heathlands
and savannahs;
b the leached soils of constant light rainfall
conditions such as laterites and those of mountain
 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
saddles where conditions of constant downward
water and nutrient movement apply (e.g. Dipteris,
Plate II, 5);
b newly formed volcanic ash surfaces ;
b post-wild¢re sites;
b erosion surfaces of lithophytic sites ;
b habitats of high metalliferous availability
such as ultrama¢c soils and man-made metallifer-
ous mine spoils;
b epiphytic habitats.
Wide arrays of fern species from diverse fami-
lies are today specialist colonists of many of these
sites, with considerable specialisations especially
of life-form between di¡erent fern families in ex-
ploiting di¡erences between each of these rela-
tively demanding situations.
For example, epiphytic habitats almost exclu-
sively require unusually high tolerance levels of
the low-nutrition suite, and subtle levels of biotic
competition are probably also involved in di¡er-
entiating between di¡erent ‘preferred’ epiphytic
substrates. Despite these limitations, an enormous
number of pteridophyte (especially fern) epiphyte
species exist. Some (e.g. species of Tmesipteris) are
themselves specialists mainly of tree-fern trunks,
even to genus (Dicksonia), while the majority even
specialise in the occupation of speci¢c branch
niche locations (often prescribed by their mor-
phology) and tree canopy heights occupied on
particular tree species hosts. The whole epiphytic
pteridophyte suite is composed of an enormous
range of morphological habits of pteridophytes,
from creeping to pendulous, and some quite bi-
zarre compost-making specialists. Many can to-
tally blanket portions of the bark of the tree on
which they grow. Some appear physically inter-
dependent, and some are symbiotically ant-asso-
ciated in obligate or facultative ways, or subse-
quently form various other animal and other pte-
ridophyte habitats. Typically they are (relatively)
fast-growers, and the duration of life of all as a
maximum is limited to that of the tree on which
they grow. Many fall in storms, often driven by
their own weight, where they die and decompose
rapidly on the forest £oor, due to combinations of
construction of many soft and semi-succulent
parts as a consequence of their growth rates.
By contrast, ultrama¢c sites clearly require un-
PALBO 2428 5-6-02
15
usual degrees of tolerance levels from both suites,
and the levels of such tolerances often appear to
be highly taxon-speci¢c. A smaller diversity of
plant habits is present, with plants usually of
small size, scattered (seldom contiguous) occur-
rence, and tough, leathery growth. Dead fronds,
frond debris and especially frond bases may per-
sist around parent plants for years. On directly
nutrient poor edaphic sites, either characterised
by post-¢reburn environments or (especially) by
erosion-regimes and constant surface moisture
downwash such as today on high-mountain sad-
dles, notably sprawling and often rampant pteri-
dophyte habits are especially characteristic, with
tough growth structure typically yielding much
local and outwash debris.
The frequency of occurrence, and the taxonom-
ic diversity, of ferns in all of these habitats today,
with subtle di¡erences between sometimes related
taxa and their adaptations, suggests a long past
history for this phenomenon. Sites of unusual
mineral availability must have always occurred,
while ¢reburn sites, some with ferns, are known
since at least the Early Carboniferous (¢de Scott
and Jones, 1994; Falcon-Lang, 1998, 1999; DiMi-
chele and Phillips, 2002-this issue). Volcanic ash
habitats, also with ferns, are known from at least
similar times (Scott and Galtier, 1985; Brous-
miche et al., 1992; Crowley et al., 1994). The
antiquity of this strategy, which probably enabled
opportunistic colonisation even among early ¢li-
caleans, is further indicated by Galtier and Phil-
lips (1996). Epiphytism amongst ferns, although
very fragmentarily known (e.g. Sahni, 1931;
Rothwell, 1991; Poole and Page, 2000) has a
very long fossil history from the Palaeozoic (Ro«ss-
ler, 2000; DiMichele and Phillips, 2002-this issue).
Survival of ancient biota collectively on such
sites seems also indicated amongst extant taxa
by the occurrence of taxonomically outlying and
presumed relictual species of ferns associated with
apparently relictual conifers as enclaves on some
heavily mineralised soils. One example is the oc-
currence of several Schizea species and the mono-
typic Stromatopteris moniliformis closely co-asso-
ciating on ultrama¢c soils in New Caledonia
(Page, 2002a,b). The exploitation of the ability
to colonise a variety of low nutrient habitats is
16 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
a strategy which is probably widespread through
the fossil record for Pteridophyta, and doubtless
has included, within its exponents, many di¡erent
groups of ferns. Many terrestrial ferns as far back
as the Early Carboniferous have ‘sprawling’ or
‘rampant’ habits (DiMichele and Phillips, 2002-
this issue) and one cannot help but note that
this habit is characteristic of extant pteridophytes
surviving on the poorest edaphic terrains.
3.5. High migrational ability of the airborne spore
The dispersal potential of the airborne pterido-
phyte spore confers on ferns the potential of un-
usually high dispersal mobility. Main advantages
arising from this appear to be:
(1) potential to continually arrive at sites of
poor access, such as rock-faces and, especially,
epiphytic sites;
(2) potential to arrive rapidly at newly arising
locations and thus pioneer habitats, such as land-
slide surfaces and new volcanic terrains;
(3) potential to achieve (however occasional)
long-distance dispersal, from continents to ocean-
ic islands or between remote island chains.
These potentials are not mutually exclusive, and
all possible combinations of one, two or all three
are clearly available. Furthermore, all are not
once-only events, but apply continuously to spore
generation and release processes in most fern
communities.
All spore dispersal achievements are described
here as ‘potential’ since to what degree they are
actually realised in nature is clearly complex and
is yet only fragmentarily understood. Many var-
iations in circumstances must apply. Exactly how
signi¢cant long-distance dispersal might be in
pteridophytes has, for example, long been a topic
of debate (e.g. Gregory, 1945; Lloyd, 1974a,b;
Parris, 1985; R.M. Tryon, 1985, 1986; Kendall
et al., 1986; Lacey and McCartney, 1994; Caul-
ton et al., 1995; Schneller, 1996b), though there
are few exacting data on this issue.
My own interpretations are based on three lines
of evidence : (1) my personal ¢eld experience of
fern £oras on oceanic islands in three major
oceans today; (2) the known longevity of wide
taxonomic arrays of fern spores in captive storage
PALBO 2428 5-6-02
(4^25 yr in packets, a maximum of 63 yr recorded
on an herbarium sheet); and (3) the known resis-
tance of fern spores to environmental hazards (see
Page, 1979b for an earlier review). These interpre-
tations, however, equate closely with those de-
rived by Cousens (e.g. Cousens et al., 1985, and
personal communications 1980^1986), also based
on independent experimental studies and parallel
¢eld observations, which included the appearance
of taxonomically novel pteridophytes along the
American Gulf Coast following episodes of hurri-
cane damage. I take a pragmatic approach and
simply begin from the practical stand-point that
all fern spores have, and always have had, oppor-
tunity to get more-or-less everywhere given time.
Sure, there will be a very rapid gradient of spore
density dilution away from the parent plant.
However, spores can also disperse in long and
steady smoke-like plumes, and once airborne,
can enjoy great resistance to known environmen-
tal hazards (see Section 3.6: Spore tolerance of
adverse aerial environments). I conclude that it
is not dispersal per se that is usually limiting in
terms of achievement of dispersal potentials in
pteridophytes (and that endless discussion of
fern-spore migration abilities is a red-herring in
terms of dispersal usually achieved). Instead, it
is the opportunities for establishment of arriving
spores, against indigenous biotic competition, that
is the real issue determining and confronting eco-
logical achievement and ultimate range: create the
appropriate habitat, and the appropriate pterido-
phyte coloniser will, sooner or later, appear there.
The likely e¡ect of distance is usually to in£uence
the timing, rather than the actuality, of the event.
In this, disturbance regimes especially promote
renewed colonisation opportunities, almost irre-
spective of where located, and biologically it is
probably those few spores that actually do get
far that are the real ecological and evolutionary
achievers.
Some genetic evidence, which appears to sup-
port these views, has been recently gained in the
case of the rare fern Dryopteris remota (Schneller
et al., 1998). Furthermore, the activeness of many
pteridophyte discharge mechanisms would appear
to have evolved particularly in response to selec-
tion pressures to optimise high mobility gain,
 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
rather than to fall near to the parent plant. Addi-
tionally, as pointed out long-ago by Manton
(1950), a single spore arriving by long-distance
dispersal must self fertilise if it is to establish a
¢rst colonising sporophyte. Most ferns appear to
have this potential (see Section 3.7: Flexibility of
breeding systems to match varying ecological op-
portunity). A genetic consequence of this is, of
course, that restoration of the diploid chromo-
some number ensures that every gene becomes
homozygous and thus phenotypically expressed
in the new sporophyte, irrespective of whether
that gene was recessive or dominant in the pre-
vious population. The haploid propagule thus en-
sures that long-distance originating founder pop-
ulations can arise which are immediately di¡erent
in detailed adaptation to those of their previous
population, and on which natural selection for
that location at that time can consequently oper-
ate. This would seem to be particularly signi¢cant
both today and through geological time in the
evolution of the fern £oras of remote sites, and
especially those of oceanic islands.
The dispersal facility conferred by the airborne
spore, creating an ever-present unseen ‘spore-
rain’, is clearly a powerful and constantly recur-
ring factor in pteridophyte ecology (Page, 1967a,
1986), and undoubtedly must have likewise have
been so virtually throughout the history of land
plants. In combination with some of the above
tolerances, perhaps the most spectacular palaeo-
examples of the ‘spore-rain’ potential have been
rapid achievement of ‘fern-spikes’ following the
great environmental disturbance events of the
Cretaceous^Tertiary and perhaps also the Trias-
sic^Jurassic boundaries (e.g. Spicer, 1989; Fowell
and Olsen, 1993; Srivastava, 1994; and see also
Collinson, 1996, 2002-this issue, for discussion).
3.6. Spore tolerance of adverse aerial environments
Virtually all of the potentials outlined above
would be negated if the fern spore was not viable
on arrival at a potential germination site. Long
distance dispersal may involve exposure to a
range of aerial extremes en route, including those
of extreme dryness, cold temperatures and irradi-
ation. Much of the earlier data on this topic (see
PALBO 2428 5-6-02
17
Page, 1979b) still remains valid. This leads to the
view that ferns spores are highly resistant to vir-
tually all of the conditions which they might be
expected to meet during the course of airborne
dispersal, even were this to be prolonged and at
high altitude.
Additional aspects of spore viability-persistence
in the ¢eld in relation to soil spore banking have
also recently been discovered in ferns (Dyer and
Lindsay, 1992, 1996; Lindsay et al., 1994).
Schneller (1996b) has further shown an important
contribution by banked spores in helping to
achieve a potential, when exhumed, of forming
many di¡erent genotypes at any location within
the population’s area. Furthermore, there is great
diversity in the architecture of fern spores (see, for
example, the many excellent illustrations of Tryon
and Tryon, 1982), yet almost nothing is known
about the adaptive and ecological signi¢cance of
their varying morphological characteristics. Some
discussion of possible functional roles of spore
ornamentation including in resistance and disper-
sal, is given by Kramer (1977) ; A.F. Tryon (1986)
and Van U¡elen (1986) and by Hemsley et al.
(1999) ^ mainly on megaspores.
Another result of extended spore viability is the
ability conferred for migration and e¡ective long-
distance dispersal. The typically high proportions
of Pteridophyta in the £oras of oceanic islands
(see Section 3.5: High migrational ability of the
airborne spore), demonstrate the e⁄cacy of this,
and may well have been one of the main selection
pressures for achievement of such viability poten-
tials. Floristic patterns between such areas in the
fossil record could well provide valuable indica-
tors of the progress of evolution of such achieve-
ment. [A review of Mesozoic, Cainozoic and mod-
ern fern biogeography (Moran, 2001) will provide
a basis for future study of this topic.]
3.7. Flexibility of breeding systems to match
varying ecological opportunity
In addition to direct ecological achievements
shown by pteridophytes, relatively complex breed-
ing systems exist which play important roles in
endowing these plants with £exibility to con-
stantly respond to environmental challenges. Three
18 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
mating-system patterns are generally recognised in
ferns: sel¢ng (1) within or (2) between prothalli of
the same parent sporophyte (intragametophytic
and intergametophytic sel¢ng, respectively) and
(3) outcrossing between prothalli arising from
the spores of di¡erent parent sporophytes (inter-
gametophytic crossing) (Klekowski, 1972a,b,
1973a,b, 1979, 1982; Soltis and Soltis, 1987, 1992).
While mating between prothalli, whether these
be from the same parent sporophyte or from dif-
ferent parent sporophytes, is clearly obligate in
hetersporous ferns, in the majority of living ferns
(which are homosporous) mating-systems are to a
high degree £exible and opportunistic. The pro-
thalli of homosporous ferns have, in general, both
male (antherdial) and female (archegonial) or-
gans. There is normally a time-phase di¡erentia-
tion between maturity of the organs of the two
sexes. However, there may also be a period of
overlap, and for most taxa, so far as is known,
either intragametophytic and intergametophytic
sel¢ng can be an option only if out-fertilisation
by intergametophytic crossing fails. Outcrossing
is thus likely to be e¡ectively realised wherever
appropriate opportunity arises, and, with certain
limitations (Schneller, 1996a), most ferns are
widely regarded as being extreme outcrossers,
with only a few nearly exclusively inbreeders
known (e.g. Ranker, 1992; Soltis and Soltis, 1992).
Where whole populations of prothalli exist,
then sexual balances amongst prothalli growing
from homosporous spores are known to be fur-
ther mediated by antheridiogens (e.g. Schneller et
al., 1990; Korpelainen, 1997), the in£uence of
which further encourages outcrossing and mini-
mises sel¢ng. In wild prothallial populations, the
e¡ects of such antheridiogens can be enhancement
of the reproductive success of small gametophytes
through promotion of gender expressions, which
would not necessarily otherwise occur (Hamilton
and Lloyd, 1991). The e¡ects of antheridiogens
can operate between prothalli of di¡erent species
in establishment of contrasting sexuality. This is
probably one of the factors promoting the num-
ber of independent congeneric hybrids which
have been ¢eld-recorded in pteridophytes (see
Rothmaler, 1944; Wagner, 1954; Walker, 1958;
Duckett and Page, 1975; Page and Barker, 1985;
PALBO 2428 5-6-02
Wagner and Wagner, 1985; Barrington, 1985;
Barrington et al., 1989; Page, 1990a,b, 1997b for
reviews).
Thus, in addition to examples of ecological in-
£uences, we also need to look at breeding systems.
These genetic potentials have probably become
increasingly varied and sophisticated through evo-
lutionary time. Nevertheless, many must be an-
cient in their basic origins and e¡ects, helping to
underpin a great diversity of fern ecological
achievements throughout the fossil record. As
with phytochemical armament (see above), there
is much work yet needed in drawing comparisons
between the breeding systems of more primitive
and more advanced living taxa and setting this
against the known fossil history and ecologies of
the groups concerned.
3.8. Revivalist tendencies of certain gametophytes
In an experiment carried out by the author
(Page, 1967b), prothalli of a range of mediterra-
nean-climate ferns of the genera Notholaena and
Cheilanthes (Sinopteridaceae) (originating from
the Canary Islands) which were tested on an ex-
ploratory basis, showed exceptional abilities to
withstand complete desiccation for enduring peri-
ods. Such desiccated prothalli were successfully
rejuvenated from a ‘crisp and dry’ completely
air-dry state after storage for many months, by
eventual return of overhead application of free
water, imitating rain.
Not all cellular sectors of each individual pro-
thallus necessarily survived such treatment, but
enough green tissue persisted in most to act as
‘revival centres’ from which new growth resumed,
and from which complete new prothalli with new
sex organs then grew. Indeed, frequently more
than a single such centre persisted in single pro-
thallus, with the result that two or more new pro-
thalli resulted where there was formerly only one.
Sexual maturity then followed, with the origin of
a completely new ‘replacement’ generation of
sporophytes. This contrasted with the young spo-
rophytes of the same taxa arising from them,
which so far as my own observations have shown,
have no comparable desiccation recovery abilities.
This glasshouse experiment con¢rmed earlier
 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
observations made independently on di¡erent spe-
cies by Pickett (1914). However, the existence of
this ability in ferns appears to have been little
appreciated and I am not aware of any other
studies that have been made since. The lack of
extensive experiment across a broad taxonomic
and habitat basis means that the extent of this
ability of pteridophyte gametophytes is unknown.
This is, however, a strategy in ferns which
could have far-reaching potentials in opening cer-
tain habitats for a range of taxa today, and which
may well have been of signi¢cance in the past.
Prothalli could succeed under moisture regimes
which are intermittent and unpredictable, on a
‘try and try again’ basis after an initial prothallial
foothold has been successfully gained. Such pat-
terns of survival could be advantageous in a num-
ber of di¡erent habitats, varying from sub-desert
sites to rock face habitats and even epiphytic
ones. In this behaviour, fern prothalli of a range
of genera are displaying a similar, if unexpected,
behaviour to mosses, suggesting that it could well
have relevance for the processes of fern-colonisa-
tion even in apparently hostile conditions, both
today and in the past.
3.9. Potential longevity of resultant sporophytes
An often overlooked advantaging strategy,
sporophyte longevity, may well be a particular
feature of more ancient plants. It is also widely
present in extant conifers (Page, 2002a,b), and
here too relatively especially so amongst many
more ancient members. In ferns, examples of
sporophyte longevity include tree ferns from 150
to 200 years (e.g. in cultivation at Penjerrick Gar-
den in Cornwall) and Osmunda plants said to be
up to 300 years old in cultivation. In the wild, the
rhizomatous fern Platyzoma is estimated to be
about 500 years old based on growth rates of 2^
3 mm per year and the diameter of the ‘fairy ring’
it had formed (Page, personal observations).
Drawbacks of vegetative longevity are perhaps
that, in contrast to species with rapid life-cycle
turnovers, rates of adaptive change are committed
to be slow. Slow life-cycle turnover may have con-
tributed to evolutionary stasis seen in several pteri-
dophyte groups (see Section 3.11: Exploitation of
PALBO 2428 5-6-02
19
potentials of polyploidy). Main achievements of
sporophyte longevity are:
(1) capitalisation on success of achievement of
the gametophyte stage and subsequent physical
retention of a hard-won niche;
(2) that maximisation of sporophyte size can be
achieved: this is important, for example, in gain-
ing frond size exposure to most dispersive air-cur-
rent opportunities;
(3) spread of spore output of genetically suc-
cessful individuals over the longest number of
years : this is of particular advantage, for example,
in achieving successful colonisation of habitats
which appear only sporadically.
Assessments of longevity in fossil pteridophytes
in relation to past selection pressures in di¡erent
environments would be valuable. However, it is
very di⁄cult to establish fern longevity in the fos-
sil record (Collinson, personal communication,
2001). One has to presume that tree ferns espe-
cially must always have been long lived and that,
amongst other Pteridophyta, horsetails must have
been similarly so. Therefore, amongst the giant
Carboniferous representatives of these plants
sporophyte longevity was probably the norm.
3.10. Exploitation of mycotrophy
Mycorrhizae have been widely recorded in as-
sociation with the roots of extant ferns in ¢eld
surveys in widely scattered locations (e.g. Burge¡,
1938; Cooper, 1976; Iqbal et al., 1981; Newmann
and Reddell, 1987; Jones and She⁄eld, 1988;
Gemma et al., 1992; Moteetee et al., 1996). This
suggests that such associations may well be a nor-
mal feature of the roots of the majority of extant
ferns as well as ancient pteridophytes (Pirozynski,
1981, 1988; Taylor, 1990). As a generalisation,
there appears to be an emerging picture that my-
cotrophy, though frequently present in the ¢eld
gametophyte and sporophyte generations, is more
obligate in more primitive (especially eusporan-
giate) taxa (e.g. Montgomery, 1990), and prob-
ably more facultative in most more advanced
(especially leptosporangiate) genera. This is sup-
ported by observations from experimental culture
which indicate that gametophytes of virtually all
leptosporangiate taxa tested will grow successfully
20 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
aseptically, but there are other claims that ‘best’
growth is achieved when prothalli have access to
normal soil fungi (e.g. Hutchinson and Fahm,
1958). Where associations are facultative, it would
seem most likely that these could most advantage
ferns either in terms of growth, perranation or in
achieving exploitation of unusual and perhaps ex-
acting ecological habitats, but remarkably little is
known about this. By complete contrast to ferns,
I know of no reports of mycotrophy in horsetails,
though experiments I have carried out growing
roots of Equisetum in aqueous culture (Page,
1967b) show that the sporophyte itself has long
and unusually persistent root hairs, which may
well function in a similar manner.
Mycotrophy in pteridophytes is signi¢cant,
however, in that it would appear to be of partic-
ularly ancient occurrence in primitive land plants
since at least the Early Devonian (e.g. Taylor,
1990; Banks and Colthart, 1993). Data linking
between past pteridophyte diversity and exploita-
tion of mycotrophy would be valuable, since such
relationships may well have provided a particu-
larly important advantaging strategy for fern suc-
cess in a wide array of habitats throughout geo-
logical time.
3.11. Exploitation of potentials of polyploidy
The contribution which the exploitation of the
potentials of polyploidy (and especially allopoly-
ploidy) has made to the achievement of speciation
in ferns has been one of the main areas of new
understanding in this group in the last 50 years
(e.g. Manton, 1950; Shivas, 1961; Walker, 1958,
1966a,b, 1979, 1985; Page, 1967b, 1973, 1997a;
Lovis, 1977; Wagner and Wagner, 1980; Werth
et al., 1985; Soltis and Soltis, 1987; Barrington et
al., 1989; Hau£er, 1989a,b, 1992; Wolf et al.,
1990, 1991; Rabe and Hau£er, 1992; Hau£er et
al., 1995). It has become clear that while autopo-
lyploidy is only an occasionally successful evolu-
tionary route in ferns, allopolyploidy is widely
successful (Walker, 1979, 1985; Hau£er, 1996).
Allopolyploidy allows for existing genomes to
be recombined in new and fertile taxa. It provides
a rapid route for species evolution and adaptation
in ferns, and, where most successful, it tends to
PALBO 2428 5-6-02
produce plants of enhanced vigour, typically re-
£ected in increased size and/or faster vegetative
growth rates. Ferns have large numbers of small
chromosomes in cells with high cytoplasmic vol-
ume ratios. This enables many stages of chromo-
some doubling to be successively accommodated
upon one another, while maintaining full opera-
tional integrity of the cells themselves during their
crucial mitotic and meiotic divisional processes.
Allopolyploid-derived tetraploids, octoploids and
ploidy levels up to 16 ploid are known, and may
be higher than this in some genera whose base
numbers are uncertain. Back-cross hybridisations,
between members of di¡erent ploidy levels within
genera, appear to be just as common as crosses
between those of the same level. The permutations
which can result are many, progressively building
complex reticulations of inter-speci¢c relation-
ships within individual genera (e.g. Wagner, 1954;
Hau£er and Windham, 1991; Hau£er et al., 1995;
Thomson, 2000).
Additional outcomes in terms of fern genetic
potentials, which may be related to ploidy levels,
include the existence of hybrid swarms (¢rst pro-
posed in Pteris by Walker (1958) and recently
con¢rmed by molecular work, for example in Po-
lystichum ^ Mullenniex et al. (1998). In addition
there are multiple hybrids at the same ploidy lev-
el, some of which produce a percentage of appar-
ently good spores (Page, 1963, 1990a, 1997b). A
mechanism for stabilisation of hybrid reproduc-
tion at a homoploid level, autogamous allohomo-
ploidy, has also been proposed (Conant and
Cooper-Driver, 1980). Opportunity also exists
for changes in mating systems, high genetic heter-
ozygosity, the survival of genetic redundancy and
the ability for species, including narrow endemics,
to store high genetic variability (e.g. Chapman et
al., 1979; Gastony and Gottlieb, 1982). Also an
initially limited gene pool of an allopolyploid may
be enriched as a result of multiple origins, muta-
tions and/or intergenomic recombinations (Werth,
1992). In established polyploids, silencing of du-
plicate gene expressions (Werth and Windham,
1991; Gastony, 1991) and practical genetic dip-
loidisation may subsequently ensue (e.g. Wolf et
al., 1987, 1990). The whole process results in the
creation of morphological and ecological novelty,
 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
genetic diversity, maintenance of fertility, and
clear separation of genetic identity between dip-
loid progenitors and polyploid derivatives. The
practical evolutionarily results are:
(1) the speed with which new taxa of ferns can
arise as pure-breeding lines;
(2) that resultant ‘instant’ taxa are each adapted
to somewhat di¡erent ecological conditions than
the parental taxa; and
(3) that such new taxa may combine new eco-
logical abilities with hybrid vigour.
In consequence, in long-stable environments, it
is likely that allopolyploids, though they may
arise, will be seldom necessarily more successful
than their parents if these are already ecologically
well-adapted. However, in more actively evolving
£oras and under more changing environments,
higher ploidy derivatives can more often ¢nd
niches clear for ecological success, probably even-
tually displacing many of the original ancestral
diploids. An extreme range of contrasts amongst
fern ploidy spectra is thus apparent. The long-sta-
ble and highly encapsulated fern £ora of the Can-
ary Islands has well under 30% polyploidy and
these only of low ploidy grades (Page, 1967b,
1973). This can be compared with the less con-
¢ned and more actively evolving fern £oras of
either post-Pleistocene deglaciated areas of Eu-
rope (e.g. Manton, 1950; Vogel et al., 1998). or
with what have been widely regarded as more
modern tropical fern £oras (e.g. Jamaica and Tri-
nidad ^ Jermy and Walker, 1985; Walker, 1966a,
1985). In these examples, over 70% polyploid rep-
resentation, including high grades of ploidy, is
more typical. The former circumstances thus
have the greatest possibility of preserving relictual
taxa in ferns (with many of the ferns of the Can-
ary Islands, for example, surviving today little
changed since the Miocene ^ Page, 1967b), the
latter for the success of much newer diversity.
Even if only some of these aspects have applied
throughout the past history of ferns the potential
conferred on ferns to meet new environmental
challenges is clearly high. These mechanisms
may well have contributed signi¢cantly and sub-
stantially to fern ecological adaptive change and
hence long-term fern survival and diversi¢cation.
Evolutionary stasis, perhaps in part involving
PALBO 2428 5-6-02
21
ploidy stability and in part related to life-cycle
longevity, has been identi¢ed in several genera
and species groups within the fossil record (e.g.
Rothwell and Stockey, 1991; Delevoryas et al.,
1992; Rothwell, 1996a; Herendeen and Skog,
1998; Phipps et al., 1998; McIver and Basinger,
1989; Serbet and Rothwell, 1999; Pigg and Roth-
well, 2001). High polyploids may be typical of
past activity in some ancient lineages, such as
Ophioglossum and Equisetum, while mechanisms
are also provided whereby opportunities for new
developments from old stocks (e.g. Page and
Barker, 1985; Ollgaard, 1992) can also rapidly
occur.
3.12. Biotic independence
Apart from mycorrhizal associations (see Sec-
tion 3.10: Exploitation of mycotrophy), and cer-
tain known examples (e.g. the genera Lecanopte-
ris, Solanopteris, Pteridium) where ferns gain
additional protection of their whole vegetative
structure by attracting ants (see Section 3.2: Di-
verse phytochemical armament), there are few
other pteridophyte^animal associations. The only
ones of which I am aware, are the spiny spores in
some Isoetes species (e.g. I. echinospora) which
appear to be an adaptation to bird dispersal
(Page, 1982b). Also some echinate spores, and
the unusual lasoo-like ¢lamentous outgrowths of
spore walls in Lecanopteris mirabilis, have been
suggested to be an adaptation to spore transport
by the sporophyte’s associated ants (A.F. Tryon,
1985, 1986). It is, however, noteworthy that only
a very few known examples exist and a certain
level of quite local evolutionary experiment seems
indicated, with methodologies which, in pterido-
phytes generally, appear not to have become
widespread.
Throughout the vast bulk of pteridophyte di-
versity, there appears to be remarkably little de-
pendence on animals in general achievement of
the main life-cycle functions of vegetative growth,
propagule dispersal or sexual achievement. Most
ferns consequently constantly ‘shun’ rather than
‘court’ most animal species. This is in great con-
trast especially to the £owering plants, where
courting of animals (especially of pollinating in-
22 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
sects by £owers) has enabled often complex and
sometimes bizarre pathways of achievement to
evolve which are presumably more e¡ective than
could be achieved without such support.
Two important advantages accrue, however, for
ferns:
(1) Having established e¡ective pathways of
biochemical defence mechanisms (see Section
3.2: Diverse phytochemical armament), there is
an uncomplicating freedom to apply these without
limitation throughout all the varied stages of the
plant life cycle.
(2) It has enabled the main life processes of
Pteridophyta, including dispersal and mating, to
be achieved virtually exclusively with the presence
of the simple physical agencies, which change lit-
tle with time.
Any partitioning of toxic e¡ects from certain
organs or life-cycle stages is thus clearly unneces-
sary if animals do not need to be courted. This
has contributed enormously to the fern’s freedom
of specialisation in defence through the develop-
ment of whole cocktails of diverse chemical
agents, against which animal groups are least
likely to evolve complete defences. For example,
in combination with other agents, the production
of insect ecdysones by ferns must be a defence to
which it is di⁄cult for an insect to evolve resis-
tance, even through geological time!
Such biotic independence today almost cer-
tainly closely re£ects a life-style which probably
began with the ¢rst vascular land colonisers.
Thereafter, through the dependence for dispersal
and reproduction solely on only uncomplicated
physical agencies pteridophytes have audaciously,
solidly and unambiguously ‘pinned their colours’
to those agencies which neither change signi¢-
cantly through time, nor become extinct. Such in-
dependence has contributed signi¢cantly to what
these plants have been able to achieve, and con-
sequently to the close comparability between
modern and fossil pteridophyte life-styles.
4. Discussion and conclusions
Very considerable pteridophyte ecological di-
versity survives today (Copeland, 1907; Holttum,
PALBO 2428 5-6-02
1938, 1954; Page, 1977, 1979a,b; Page and Clif-
ford, 1981; Johns, 1985), with over 12 000 species
of ferns alone. In terms of species richness, homo-
sporous pteridophytes are more successful than all
other non-angiosperm grades combined (Roth-
well, 1996a). This account demonstrates that,
amongst pteridophytes, similar general responses
are shown time and time again by distantly re-
lated taxonomic groups in response to similar se-
lection pressures. Using knowledge of the ecology
(especially autecology, life-cycle biology, environ-
mental interrelationships and adaptations) of
ferns and fern allies today, an attempt is made
to analyse why pteridophytes are able to colonise
such a range of habitats, and especially so many
marginal ones. This synthesis is used to derive
basic principles concerning the innate biological
weaknesses (limitations) and special strengths (ad-
vantages) of Pteridophyta as a whole, which are
presented here.
The seven limitations identi¢ed are innate
weaknesses of pteridophytes, which clearly limit
fern potentials and achievements today. Clearly,
none of these have been able to be successfully
‘thrown-o¡’, to any major degree, in the course
of pteridophyte evolution. On this evidence, all
must have acted as similar limitations throughout
pteridophyte evolutionary history. Interestingly,
few of these (perhaps only the single growing
point (Section 2.2: Single growing-point limita-
tions of sporophyte architecture)) might be de-
duced directly from the fossil record itself, and
most would therefore be unknown if we did not
have evidence from the living plants.
By direct contrast, the 12 advantages conserva-
tively identi¢ed (14 if including subcategories
within Section 3.2: Diverse phytochemical arma-
ment, and Section 3.4: High tolerance of acute
nutrient disequilibrium substrates) clearly open
opportunity for exploitation of a considerable ar-
ray of ecological habitats by pteridophytes today.
Many have the ability to operate in varying de-
gree, with a range of subtle variations in e¡ect.
Virtually all have the potential to operate in com-
binations, helping to explain the ecological diver-
sity which pteridophytes, and especially ferns,
have achieved. Experimental evidence indicates
that most of these advantages appear broadly
 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
across most taxonomic groups and seem to have
deep-rooted origins within Pteridophyta, to the
degree that many are judged to be special innate
abilities of these plants. On this evidence too,
most must have also been available to operate
throughout pteridophyte evolutionary history.
Some, such as tolerance of extremes of edaphic
conditions, may have actually directly helped sur-
vival of several ancient fern genera to occur
(Page, 2002d). Interestingly again, a few might
be proven, some others inferred, but many would
also remain unknown, especially in the potentials
which they liberate, if we did not have evidence
from the living plants.
The 12 advantages help to mitigate, to tolerate,
and sometimes to positively exploit, the worst ef-
fects of the seven limitations in a number of ways.
For example, the handicap of an independent ga-
metophyte stage, the poorly controlled evapora-
tive potential, and the need to ‘return to the water
to breed’ are all to a degree o¡set by the abilities
conferred by high disease resistance under satu-
rated humidity levels. Upon this balance, low-
light photosynthetic abilities then enable many
such high-humidity but necessarily low-illumina-
tion habitats, in which biotic competition levels
are generally low, to become exploited to the
full. Slow plant growth rates may be less of a
handicap under these often most stable of condi-
tions, while mycotrophic exploitation in gameto-
phyte and sporophyte generations doubtless fur-
ther supports survival in these and many other
marginal habitats. Intolerance of widely £uctuat-
ing conditions by the sporophyte is, in appropri-
ate habitats, partly o¡set by the revivalist tenden-
cies of certain gametophytes. The single growing-
point limitations of sporophyte architecture are
partly o¡set by many speci¢c morphological
adaptations of genera. These are augmented fur-
ther by ecological escapism of many ferns to hab-
itats which are either too remote (e.g. epiphytic)
or too toxic (e.g. heavily mineralised substrates)
for plant and animal pressures to be intense.
These habitat opportunities are especially pro-
moted by the unusual tolerance levels of ferns
for sites of acute nutrient disequilibrium as well
as the access to these regularly gained by the high
mobility of the airborne spore. Animal browsing
PALBO 2428 5-6-02
23
is also targeted by the diverse phytochemical ar-
mament of pteridophytes, which has a broad
spectrum of e¡ects on animals, especially against
invertebrates. Uncontrolled high reproductive
commitment, although doubtless a highly en-
ergy-intensive process, is combined with potential
longevity of resultant sporophytes. Together these
attributes are e¡ectively exploited by the high mi-
grational ability ( = potential dispersal) of the air-
borne spore, coupled with the known spore toler-
ances to adverse environmental circumstances.
The breeding systems and their diversity are
clearly consequent on dispersal opportunities, no-
tably the facultative inbreeding fallback when
outbreeding fails which enables e¡ective long dis-
tance dispersal by a single spore. Today pterido-
phyta also gain ecological adaptation and evolu-
tionary advantage from their extensive
exploitation of potentials of polyploidy (especially
allopolyploid progression) and their high degree
of biotic independence. It is inferred that these
are also attributes with a long past history.
Amongst living pteridophytes, ancient elements
as well as modern elements often co-exist (Stewart
and Rothwell, 1993). Many fern families, notably
Marattiaceae, Osmundaceae, Schizaeaceae, Glei-
cheniaceae, Matoniaceae, Dipteridaceae, Dick-
soniaceae, Cyatheaceae, Azollaceae, Salviniaceae
and Marsileaceae, have well established, extensive
fossil records (Collinson, 1992, 1996, 2002-this is-
sue ; DiMichele and Phillips, 2002-this issue ; Van
Konijnenberg-van Cittert, 2002-this issue). Other
non-fern pteridophytes, especially Equisetaceae
(Page, 1972a,b), Selaginellaceae (Page, 1989) and
Lycopodiaceae (Wikstro«m et al., 1999) show evi-
dence of adaptive traits which must also have oc-
curred in the past biology, ecology and ancient
morphologies of these groups. Periods of evolu-
tionary stasis have been recognised, either from
the fossil record of single species such as those
of Osmunda, Onoclea and Woodwardia (e.g. Roth-
well and Stockey, 1991; Rothwell, 1996a; Phipps
et al., 1998; Serbet and Rothwell, 1999; Pigg and
Rothwell, 2001), or in whole pteridophyte £oras
from their surviving cytology (Page, 1967b, 1973).
Similarly, there may be little change in at least
some generic a⁄nities with habitats through
time. Examples certainly include Onoclea, Osmun-
24 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
da and Woodwardia, which appear to have had
members associated closely with swamp habitat
margins similar to those of today since the Ter-
tiary or earlier (e.g. Rothwell and Stockey, 1991;
Greenwood and Basinger, 1994; Pigg and Roth-
well, 2001; Collinson, 2002-this issue); Equisetum
with similar habitats for at least as long (McIver
and Basinger, 1989) or very much longer (Page,
1967b, 1972a); Acrostichum, characteristic today
of (uniquely) humid-tropical brackish-water es-
tuaries and swamps, and spreading into the sea-
ward-face of mangrove swamps today, clearly as-
sociated with lakes and freshwater marshes in the
Cainozoic (Collinson, 2002-this issue); free-£oat-
ing water ferns (Azolla and Salvinia) in freshwater
facies with a range of associated aquatic angio-
sperms widespread in the Cainozoic (Collinson,
2002-this issue); and gleicheniaceous and schi-
zaeaceous ferns as opportunists colonising open
and disturbed ground including ¢reburn sites
and volcanogenic terrains since at least Mid-Cre-
taceous (Collinson, 1996, 2002-this issue ; Van
Konijnenberg-van Cittert, 2002-this issue). More
contentious (Collinson, 2002-this issue) at present
is the claim (Poole and Page, 2000) of a probable
Eocene epiphyte of Polypodiaceous a⁄nity,
though I maintain my conviction: if there are
Polypodiaceae and there are trees, then there are
epiphytes (though I do not dispute that additional
evidence of these in physical connection would be
valuable!). Fern epiphytes are proven in Palaeo-
zoic £oras, attached to tree fern trunks (Ro«ssler,
2000; DiMichele and Phillips, 2002-this issue).
The ecology of living pteridophytes shows that
this group is both complex and dynamic, and that
these complexities still confer great versatility,
£exibility and adaptive e¡ectiveness, especially
through their abilities of exploiting an unusually
wide range of marginal habitat conditions. Ferns
have, in consequence, achieved long-term surviv-
al, diversi¢cation and success through evolution-
ary time. Although primitive forms persist, diver-
si¢cation continues to occur on the basis of not
only modern stocks (e.g. Wagner, 1954; Hau£er
and Windham, 1991; Hau£er et al., 1995) but also
on already ancient ones (e.g. Page and Barker,
1985; Page, 1972b, 1990a, 1997b; Ollgaard,
1992, 1996). Great evolutionary £exibility and re-
PALBO 2428 5-6-02
sponsiveness, organisation and ecology have also
been emphasised within the Pteridophyta from a
fossil perspective since the Palaeozoic (DiMichele
and Phillips, 2002-this issue), and a diversity of
habitats has been occupied through the Mesozoic
(Van Konijnenberg-van Cittert, 2002-this issue)
and Cainozoic (Collinson, 2002-this issue). All
of these alternatives will have operated, perhaps
with varying emphases and in varying degrees,
between times of relative evolutionary quiescence
versus periods of more active radiation (Collin-
son, 1991, 1996; Rothwell, 1987, 1999).
Today their living survivors provide evidence of
the diversity of the innate mechanisms and pro-
cesses which ferns are able to develop and exploit,
and the diversity of adaptations and ecological
potentials which can thereby be achieved (Page,
1997a, 2000, 2002c). These same innate mecha-
nisms and processes must have similarly occurred
throughout much of pteridophyte fossil history,
opening similar ranges of adaptations and ecolog-
ical potentials, as strategic elements of recurring
pteridological achievement.
Although drawing comparisons between living
Pteridophyta and fossil ones is far from new,
most such comparisons have been largely fossil-
driven, and relate usually to speci¢c fossil taxa or
habitats, seeking their modern equivalents for
comparison. Particularly important recent synthe-
ses have been made in this perspective by, for
example, Rothwell (1987, 1991, 1996a,b, 1999).
The approach presented here is proposed as com-
plementary to that which can be gained from the
fossils themselves. It is argued that the modern
fern ecologies help to point to a diversity which
could (and probably did) exist in Pteridophyta at
many times in the past. Using the same strategies
as their modern analogues, ancient ferns, at many
di¡erent times and locations, and with both sim-
ilar and many di¡erent taxa to those of today,
have been similarly enabled to exploit a range of
habitat miches as wide as those seen today.
Acknowledgements
On practical aspects, I am grateful for the
support of several generations of horticultural
 C.N. Page / Review of Palaeobotany and Palynology 119 (2002) 1^33
staff at the Royal Botanic Garden, Edinburgh,
UK, for the day-to-day maintenance of my many
pteridophyte and conifer experimental cultures for
over more than 30 yr, and those at Oxford, UK,
Brisbane, Australia, and Newcastle, UK, Univer-
sities for extended periods before this. I am also
grateful to the Royal Botanic Gardens, Kew and
the Natural History Museum, London, for access
to herbarium materials, and to the Linnean
Society and Camborne School of Mines, Univer-
sity of Exeter, for access to library facilities in their
charge. On scientific aspects, discussions in the
laboratory, the field and the glasshouse, with Dr.
Trevor Walker, Clive Jermy, Dr. Heather McHaf-
fie, Dr. Adrian Dyer and Dr. Richard Bateman
have been long-term stimuli to the overall devel-
opment and progress of these studies and to many
of the ideas contained therein. Dr. Heather
McHaffie (Edinburgh, UK) has kindly provided
additional pteridological comments and Dr. Mi-
chael Proctor (Exeter, UK) ecological comments
on the resulting manuscript. I am further grateful
to Dr. Margaret Collinson for her enthusiasm and
support in helping to bring my neobotanical
concepts into a palaeo-botanic arena, and to her,
Dr. Kathleen B. Pigg and Dr. Paul Kenrick for
many helpful and constructive comments on the
resulting manuscript from a palaeo-botanic per-
spective. This paper is dedicated to the memory of
the late Professor Robert M. Lloyd (Athens, OH,
USA), the late Dr. Michael I. Coussens (Pensaco-
la, FL, USA) and the late Professor Jan Kornas
(Krakow, Poland) all of whom contributed, in
discussions and joint fieldwork, to the formation
of some of the ideas included here.
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