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Riolo~ical.Journal a/ l/w Linnenn So&& (1989), 36: 227--249. With 4 figures
The tortoise and the hare: ecology of
angiosperm dominance and gymnosperm
persistence
W. J. BOND*
Deparlmenl
of
Biology, Uniuersig of Culzfornin,
1.0s
Angeles CA90024, U.S.A.
Krceiued 15 SrplemhPr 1988. nrrrpled Jbr puhlzcativtr 6 April I988
Gymnospernis, and conifers in particular, are somctimes vrry productive trees yrt angiosperms
dominate most temperate arid tropical vegcAtation. Current explanatioirs for angiosperm success
crnphasize the ad\aiitages of insect pollination and seed dispersal by animals for the colonization of
isolatccl habitats. DifTcren(.es hctwern gymnospcrm and angiosperm 1-cproductive and vegctativr
growth ratcs have bern largely igniircd. Gymnosperms arc all woody, perennial a nd usually have long
reproductive cycles. 'l'hcir leavrs arc i i ~ as
t fully vascularized as those of angiosperms arid are more
stereotyped in shapc and size. Gymnosperm trachcids are gc-ncIally more rcsistant to solute flow than
angiosperm vessels. A consequence o f t h e lc-ss eflicicnt transport system is that maximum growth rates
of gymnosperms are lower than maximum growth rates of angiosperms i i i well lit, well watered
hahitats. Gymnosperm sccdlings may hc particularly uiicompctitive sincc their growth depends on a
single cohort of relatively inefficient leaves. Later, some gymnosperms attain a higher productivity
than co-occurring aiigiosprrm trees b y accumulating sc-veral cohorts oflcavcs with a higher total leaf
arm
'l'ticsc functional constraints o n gymnosperm growth rates suggest that gymnosperms will be
restricted to areas wherr growth of angiosperm competitors is reduced, for example, by cold or
nu trierit shortages. Biogeographic evidence supports this prediction since conifers are largely
confined to high latitudes arid elevations or nutrient-poor soils. Experimental studies show that
competition in the regeneration niche (between conifcr seedlings and angiosperm herbs and shrubs)
is conimon and significantly allrrts conifer growth and survival. Fast-growing angiosperms,
especially herbs and shrubs, may also change the frcquency of disturhancc regimes thereby
excluding slower-growing gymnosperms.
Shade-tolerant arid early su(
.ioiial conifers sharc similar c1iarartrristic.s of slow initial growth
aiid tow plasticity t o ;I chaiigr in rcsources. Shade-tolerant gymnosperms would he cxpected to occur
only where forest opcnings are small or otherwise urisuitablc for rapid filling by fast-growing
angiospcrm trees, lianas o r shrubs. 'I'he limited evidence availahlr suggests that shade-tolerant
conifers a r c confined to forests with small gap sizes where large disturbances are very rare.
' I h e regeneration hypothesis for gymnosperm exclusion by angiosperms is consistent with several
aspects of the fossil record such as the early disappearance of gymnosperms from early successional
mvironnients wherc competition with angiosperms would have heen most scvcre. However there are
unresolved dilficulties in intrrprrting process from paleoecological pattern which prevent the testing
of alternative hypotheses.
KEY WOKDS: ~Angiospcrnievolution
~
gymnosperm evolution
-
conifcr hiogrography
~
plant
conipeti tion.
CON'I'EN'I'S
Introduction .
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Characteristics ofangioslicrms versus gymnosperms ,
Reproductivc ratcs
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* Present Addrcss: Department of Botany, University of Cape 'l'own, Private Bag, Rondehosch 7700, South
Africa.
0024-4066/89/030227
+ 23 $03.00/0
227
0 1989 T h e Linnean Society of London
W. J. BOND
230
TABLE
1. Net production of angiosperm and gymnosperm forest
types measured in the same vicinity (within a radius of a few km).
N = Number of stands
Forest type
Japan (Satoo & Madgwick, 1982)
Angiosperm
Batula maximowiziana
Populus dauidiana
Gymnosperm
Picea abies
Abies Jachalinensis
Larix leptolepis
Germany (Schulze et al., 1977)
Angiosperm
Fagus syluatica
Gymnospcrm
Picea abies
N
Age Net production
(yrs) (ton ha-’ yr I)
3
1
47
40
4.2-6.2
8.7
4
1
1
45-47
26
21
1
120
4.2
1
89
8.4
7.3-12.4
13.0
16.5
American deserts, may dominate diverse geographic areas alongside large genera
with many species (e.g. Ceanothus, Arctostaphylos, Opuntia). I n this paper I am
concerned only with those features of angiosperms which led to their ecological
ascendance, in some habitats, over gymnosperms. The measure of success is
relative cover or biomass, rather than number of species.
Most recent authors have explained angiosperm advances in the past and the
restricted distribution of conifers in the present on the basis of differences in
pollination and dispersal potential (Crepet, 1984; Tiffney, 1984; Burger, 1981;
Regal, 1977). Many angiosperms are insect-pollinated while nearly all
gymnosperms are wind-pollinated. The competitive advantages of insect
pollination are said to be: (1) reliable directional pollination which costs less
energy, (2) production of outcrossed offspring in sparse populations and (3)
successful pollination where wind is ineffective (Crepet, 1984). Insect pollination
is thought to be particularly advantageous in sparse populations as insects may
carry pollen greater distances more effectively than wind (Whitehead, 1969;
1983; Burger, 1981; Regal, 1977, 1982). Thus insect-pollinated (and animaldispersed) angiosperms ought to be able to maintain gene flow over a wider
range of population sizes and structures than wind-pollinated (and winddispersed) conifers. Proponents of the pollination hypothesis explain the
widespread persistence of gymnosperms as dominant components of
contemporary vegetation by linking site to species diversity. Conifers persist
where they do, it is argued, only in dense monospecific stands where wind
pollination is as effective as insect pollination. Monospecific stands or low
diversity communities, in turn, are caused by ‘stressed’ (cold, nutrient-poor)
habitats (Regal, 1977; P. Raven, 1977; Whitehead, 1969).
There are several difficulties with this hypothesis. First there is no empirical
base for the generalization that gene flow between populations is greater in insect
than in wind-pollinated species. Studies of intrapopulation gene flow are common
but there are very few studies of gene flow between populations. Ellstrand &
Marshall (1985) could find only three, excluding their own, and caution that
generalizations on “the importance of gene flow as a cohesive evolutionary force”
ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE
23 1
between populations cannot be made at present given this limited empirical base.
Conifers, like most trees, are usually highly heterozygous (Brown, 1979; Hamrick,
Linhart & Mitton, 1979) regardless of whether species ranges are continuous or
divided into isolated ‘islands’ (Hiebert & Hamrick, 1983). At first sight this may
seem to negate the hypothesis that wind pollination reduces outcrossing. However
it can be counter-argued that natural conifer populations are already sufficiently
dense to allow adequate gene flow. The only way of studying the hypothesized
limitations of wind pollination is by explicitly searching for density dependent
effects on gene flow. Some conifers do show density dependent changes in
outcrossing rates and greater survivorship of heterozygous seedlings (e.g. Farris &
Mitton, 1984), but no studies directly compare the effects of density on
heterozygosity in both insect and wind-pollinated species. Nor would it be easy to
devise a test which isolated pollination mode from other ecological factors which
determine genetic structure (Loveless & Hamrick, 1984). A few conifers are
homozygous or nearly so, including both narrow endemics (Pinus torreyana Parry
ex Carr) and widespread species (Pinus resinosa Ait., Thujaplicata Donn ex D.Don).
Thus some conifers can survive and even thrive despite inbreeding and low
genetic variability (Ledig & Conkle, 1983).
Even if insect pollination could be shown to maintain greater genetic variation
at low densities, it does not follow that heterozygosity necessarily influences
survival and distribution of a species as opposed to fitness of genotypes within a
species. Biogeographers generally interpret vegetation patterns on the basis of
differences in growth rates, deciduosity, rooting patterns, dispersal abilities,
longevity, shade tolerance etc. (e.g. Daubenmire, 1978). Relative heterozygosity
of competing species has seldom (ever?) been identified as an important factor.
While there may, ultimately, be a link between pollination mode, population
structure and genetic variation, and even between heterozygosity and ecological
dominance, it seems reasonable to look for other more direct causes of conifer
distributional limits.
Here I argue that the competitive ability of gymnosperms is limited by rates of
both vegetative and reproductive processes rather than by access to or selection of
mates. The angiosperm innovation of the herbaceous habit (rapid foliage
production, minimal expenditure on woody support, short reproductive cycles)
allows far more effective exploitation of ephemeral habitats than the woody habit
of all gymnosperms. Angiosperms disperse as seeds rather than spores and so
escape the ecological constraints of the free-living gametophyte stage of their
herbaceous precursors, the homosporous ferns. Angiosperm herbs and shrubs
compete directly with gymnosperms regenerating in forest gaps. Although
gymnosperm (especially confer) productivity can be very high, the photosynthetic
capacity of individual leaves is low. The high productivity of some taxa is due, in
part, to a large leaf area resulting from the accumulation of cohorts of leaves over
a number of years (Waring & Franklin, 1979; Chabot & Hicks, 1982; Schulze et
al., 1986). However the seedlings of conifers possess only a single cohort of leaves
with which to compete with angiosperms in the early stages of the life of the tree. I
argue that, because of these ontogenetic constraints, conifers are restricted to sites
or successional stages which lack intense competition in the regeneration phase. I
call this the ‘slow seedling’ hypothesis. The historical implications of the
hypothesis are that the Cretaceous and Tertiary retreat of the gymnosperms was
caused by the invasion of angiosperms into the gymnosperm regeneration niche.
232
W. J. BOND
I first discuss the functional significance of apomorphic features of angiosperms,
especially those which influence vegetative growth. I then relate the functional
characteristics of modern angiosperms and gymnosperms to the niches they
occupy and thus to their biogeography. Finally I discuss whether the “slow
seedling” hypothesis is at all compatible with the fossil record of angiosperm
advances and gymnosperm declines and what alternative hypotheses successfully
explain modern gymnosperm distributions. My argument centres on conifers both
because they are by far the most successful modern gymnosperms and because
they are the most studied. For the same reasons my discussion centres on conifers
with gap-phase regeneration though I briefly consider the ecological implications
of the same functional constraints for shade-tolerant gymnosperms.
CHARACTERISTICS OF ANGIOSPERMS VERSUS GYMNOSPERMS
Reproductive rates
Among the seed plants, the potential for prolific reproduction and rapid
colonization are pre-eminent angiosperm traits. Many of the reproductive
apomorphies which distinguish angiosperms from gymnosperms are associated
with a reduction in the costs of reproduction and an increase in the reproductive
rate (reviewed by Stebbins, 1974, 1976). The style, for example, facilitates the
growth of the pollen-tube while a t the same time selectively filtering pollen
parents (Stebbins, 1976; Mulcahy, 1979). The annual herb epitomizes the
angiospermous traits of rapid growth and short generation times; some desert
annuals complete their entire life cycle in less than a month (Went, 1948). Most
angiosperms produce mature seed within a few weeks or months after flowering,
though some woody trees take a year or more, for example Quercus spp.,
Eucahptus regnans (Willson & Burley, 1983; Ashton, 1975).
In contrast, most gymnosperms have long reproductive cycles. The period from
pollination to fertilization usually exceeds 12 months (Stebbins, 1976; Willson &
Burley, 1983). All gymnosperms are perennial and all are woody trees, shrubs or
(rarely) vines. Perenniality and woodiness is related to the slower rates and
greater costs of reproduction but also to the limitations of the vegetative body
(Stebbins, 1976).
Vegetative growth rates
T h e leaf
The vegetative attributes of angiosperms include the capacity for very rapid
growth which in turn is associated with a remarkable diversity of foliage form and
function. The functional basis for rapid growth lies partly in the evolution of new
features related to the conducting system (Carlquist, 1975; see Niklas, 1985;
J.A.Raven, 1977 for the importance of the conducting system in early
tracheophyte evloution) . The earliest evidence, other than pollen, for angiosperm
divergence is the appearance of fossil leaves with complex, branching veins (Doyle
& Hickey, 1976; Hickey & Doyle, 1977). Angiosperm, and especially dicot, leaf
venation is distinctly different from conifers in the degree of vascularization with
anastomosing (closed) systems of veins and a dense network of minor veins ending
blindly in small partitions of the leaf (Foster & Gifford, 1974; Esau, 1965). Veins
ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE
233
increase the rate of solute flow through the leaf by several orders or magnitude
relative to an equivalent cross-sectional area of cell wall (Jones, 1983: 74). The
enormous conductive capacity of the leaf has been experimentally demonstrated
by severing major veins and observing subsequent tissue death in a number of
dicot leaves (Fig. 2) (Wylie, 1938; Plymale & Wylie, 1944). Gymnosperm leaves
lack the network of anastomosing major and minor veins and presumably,
therefore, have lower rates of solute transport than angiosperms*. No
comparative physiological work appears to have been done on the topic.
The major veins are structurally important in supporting the broad, but very
thin, leaf lamina. Givnish (1979) discussed mechanical aspects of leaf venation
emphasizing the cost of a vein versus its support function. Thick sclerophyll
leaves have few or disorganized veins per unit area since the thickened cell walls
are self-supporting. However sclerophylly also enables leaves to resist collapse
under highly negative water potentials where an efficient conducting system
would be superfluous (Mooney & Dunn, 1970).
The slender evidence available thus suggests that the leaf venation of
angiosperms makes possible rapid growth and expansion of leaves through
efficient supply of water. In addition the support provided by the organized
system of major veins permits a much greater diversity of leaf shapes and sizes and
greater leaf area per unit carbon expended than those seen in gymnosperms
(Doyle & Hickey, 1976). Leaf size, shape and texture in gymnosperms, in
contrast, reflect the inability of the transport system to supply rapidly expanding
photosynthetic tissue. None of the extant Coniferales, Ginkgoales, Gnetales or
Taxales have compound leaves which, in angiosperms, can act as ‘throwaway’
branches for exploiting light gaps in productive environments (Givnish, 1978).
T h e only extant gymnosperms with compound leaves, the cycads, have leaves
that are slow growing, long-lived and sclerophyllous (Chamberlain, 1934).
Conifer leaves are nearly all linear, needle or scale-like so that extension of
canopy volume depends on the growth of new shoots rather than deployment of
leaves. Conifers with broad leaves (e.g. some species of Agathis, Araucaria,
Podocnrpus) are no exception since their leaves are sclerophyllous and long lived.
The remarkable survival of Ginkgo, almost unchanged since its origins in the
Triassic, seems to have been unexploited by comparative ecophysiologists. Ginkgo
has broad deciduous leaves but non-reticulate venation. One would therefore
predict slower rates of initial leaf expansion and subsequent solute transport than
deciduous broad-leaved angiosperms. This, coupled with its architecture of
branches with short shoots, would result in a slow pace of change in Ginkgo canopy
geometry which would place it at a competitive disadvantage in broad-leaved
angiosperm forests.
Gnetum is the single gymnosperm exception with broad leaves and anastomosing
veins indistinguishable from a dicot leaf. T h e genus, which has efficient
angiosperm-like conducting vessels (Chamberlain, 1934), is also exceptional in
including the only gymnosperm lianas and is perhaps the only gymnosperm group
which thrives in angiosperm-dominated lowland tropical rainforest (e.g. Gnetum
gnetoides). Recent cladistic analysis suggests that the Gnetales are a sister group of
* Several Mesozoic gymnosperms, such as the Caytoniaceae (Sqenopleris) and some cycadophytes, show a
single order of reticular venation in the leaves. For this reason some have been suggested as angiosperm
precursors (Hickey & Doyle, 1977; Doyle, 1977).
W. J. BOND
234
A
C
B
D
Figure 2. The effects of restricted conduction on deciduous angiosperm leaves (redrawn from Plymale
& Wylie, 1944). Dotted lines indicate experimental cuts through the blade. Stippled areas are
portions of dead lamina. A, Liriodendron tulipifera; B, Quercus velutina; C , Cercis canadensis; D, Quercus
macrocarpa.
the angiosperms (Doyle & Donoghue, 1986) and evolved in parallel with (but
were never as widespread as) the angiosperms (Upchurch & Crane, 1985).
The stem
Rapid vegetative growth depends, in part, on the rate of supply of water to
leaves and meristems (Waring, 1983). Xylem is specialized into separate support
and conductive tissues in angiosperms whereas gymnosperm tracheids serve both
functions. The water conducting unit in almost all angiosperms is the vessel
whereas the tracheid serves this function in almost all gymnosperms and ferns.
Vessels offer less resistance to water flow than tracheids because they lack end
walls and are much larger (Carlquist, 1975). T h e lumen diameter of vessels
usually exceeds that of tracheids. T h e lumen diameter of conifers seldom exceeds
30-50 microns in diameter whereas diffuse-porous vessels of angiosperms
approach 100-200 microns and ring-porous vessels may be as large as 500 microns
ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE
235
(Zimmermann & Brown, 197 1; Carlquist, 1975). Conductivity is determined by
lumen diameter, total conducting area and resistance of the conducting elements
to water transport. The significance of the first two can be assessed by the HagenPoiseuille equation. If conducting elements are equivalent to cylindrically shaped
capillaries then the rate of flow over a cross section of stem, J, is given by
J = (xdi2/8n).(dP/dL)
where di is the diameter of vessel i, n is the viscosity of water and dP/dL is the
pressure potential gradient (Zimmermann & Brown, 1971; Zimmermann, 1983;
Nobel, 1983; Gibson, Calkin & Nobel, 1984). The rate of flow is proportional to
the vessel diameter squared so that, for an identical cross-sectional area, a 10-fold
increase of vessel diameter (e.g. 10 microns to 100 microns) would increase flow
rate 100-fold. The equation also shows that large diameter vessels in a stem will
transport most of the water. For example, under the same pressure gradient, a 200
micron diameter vessel adjacent to a 50 micron vessel would carry 94% of the
total volume transported through both vessels (Zimmermann, 1978). Wood cells
are not ideal capillaries but several studies have shown that the Hagen-Poiseuille
equation is a reasonable approximation of relative water flow (Zimmermann &
Brown, 1971: 199; Gibson et al., 1984).
Discrepancies between predicted and observed hydraulic conductance have
been attributed to resistance of the conducting elements. The main components of
this resistance in fern tracheids are aperture shape, length of the tapered section
and pit membranes all of which vary in relative importance depending on the
diameter of the tracheids (Calkin, Gibson & Nobel, 1986). Comparative studies
of this nature on gymnosperm and angiosperm conducting elements are needed
for determining the hydraulic significance of differences in vascular anatomy.
The maximum vessel diameter is constrained by a trade-off between efficiency
and safety since a more efficient conducting capacity involves greater risk of
accidental embolism (Zimmermann, 1971, 1978; Carlquist, 1985). Not all trees
have very large vessels because the failure of a large vessel by accidental embolism
would cut off a proportionally very large fraction of the water supply. I n general,
therefore, trees with safer, narrower vessels occur in water stressed areas or are
evergreens which suffer severe seasonal moisture stress. Large diameter vessels
typically occur either in deciduous species which replace the embolized
conducting system annually before the flush of new leaves or in evergreen species
in non-seasonal humid areas which seldom experience moisture stress (Rury &
Dickison, 1984; Zimmermann, 1978, 1983; Carlquist, 1975).
I n summary, conifer conducting systems both in the leaf and the wood are less
efficient than those of angiosperms. The large vessels and heavily vascularized leaf
of angiosperms together allow rapid transpiration and much faster growth of leafy
canopies but only where there is no shortage ofwater or the necessary nutrients for
production of new leaves. If water is seasonally deficient, temperatures freezing or
nutrients limiting, then the gymnospermous combination of narrow tracheids or
stress-tolerant, weakly vascularized evergreen leaves is a much safer alternative.
Photosynthesis and productivity
Conifers, because of the limitations of their transport system, should have lower
rates of maximum dry matter production than herbaceous or deciduous
W. J. BOND
236
TABLE2. Maximum mean values for relative
growth rates of angiosperm herbs and tree seedlings
versus conifer seedlings (ex Jarvis & Jarvis, 1964).
RGR = relative growth rate = (lnW2 -InWl)/t,
where Wi = dry weight at time i, t = time interval
RGR
Growth form
Herb
Helianlhus annuus
Deciduous broad-leaf
Betula verrucosa
Pofiulus lremula
Conifer
Pinus Vlvestris
Picea abies
(mg g-
I)
As yo of
Helianthus
980
100
513
502
52
51
81
34
8
3
angiosperms under non-limited growing conditions. When measured over short
periods, herbaceous angiosperms do have a much higher relative growth rate
than either woody angiosperms or gymnosperms (Table 2) (Jarvis & Jarvis,
1964; Grime & Hunt, 1975; Whitmore & Wooi-Khoon, 1983). Conifer seedlings,
in turn, have lower relative growth rates than deciduous woody angiosperm
seedlings (Jarvis & Jarvis, 1964; Pollard & Wareing, 1968; Whitmore & WooiKhoon, 1983; Krueger & Ruth 1969).
These differences in productivity (annual increment of dry matter) can be
attributed to differences in four growth parameters: the net photosynthetic rate
(Ps), the total area of leaf exposed per unit ground area (LAI, leaf area index),
the duration of the leaf crop (LD), and the allocation of photosynthate to leaves
or non-photosynthetic tissue (Mooney & Gulmon, 1983j . Much photosynthetic
research has focused on Ps. Photosynthetic capacity is generally reported as
being lower in conifers than in herbs or broad-leaved trees (90.8-136.2pmol
CO,m-*s-' in conifers versus 227-3 17.8 pmol CO,m-'s-' in broad-leaved trees
(Larcher, 1980; but see Nelson, 1984 for a dissenting view). However there is no
simple relationship between productivity and assimilation rate because the
annual rate of carbon gain is a product not only of Ps but also of LA1 and LD.
Schulze et al. (1977) made a detailed comparison of Picea abies and Fagus syluatica.
Photosynthetic rates were two to four times higher in the leaves of the deciduous
Fagus, but Picea, an evergreen, had four or more cohorts of leaves present
simultaneously and had a longer growing season. The net result was that Picea
stands yielded 14.9 tons C ha-' as opposed to 8.6 for Fagus in an average year.
Thus although there is a lower carbon gain per unit leaf mass in the conifer, Picea
exceeded the broad-leaved tree in annual carbon gain because the conifer
photosynthesized for a longer growing season with a much greater total leaf
biomass. Defoliation experiments have confirmed the importance of older
cohorts of leaves in evergreen conifers. For example, growth of Pinus radiata
saplings was reduced by 51% after removal of 1-2 year old leaves (Rook &
Whyte, 1976).
Because productivity of evergreen conifers depends on their accumulating a
large leaf biomass by adding successive cohorts of leaves, young conifer stands
should take longer to reach maximal leaf areas than broad-leaved stands.
ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE
237
Time
Figure 3. Hypothetical growth rate of evergreen (EG) versus deciduous (DD) trees. The two growth
forms reverse productivity from juvenile to mature life stages. B = Growth index, e.g. biomass, height.
Available evidence suggests this is the case. The maximum leaf area in deciduous
forests of the eastern United States is re-established within five years after
disturbance while Scottish plantations of Picea sitchenis take 16 years, Swedish
plantations of Pinus syluestris take 25 and the leaf area index of newly established
conifer stands in the Pacific Northwest continues to rise for 40 years or more
Uarvis & Leverenz, 1982: 250). Consequently in the early growth stages juvenile
conifers will have less foliage and less carbon income than angiosperm
competitors to allocate to shoot growth, root growth and anti-herbivore defences
especially in productive habitats. Later, as evergreen leaves accumulate, conifer
productivity frequently exceeds that of deciduous angiosperms (Fig. 3 ) .
ECOLOGICAL CONSEQUENCES OF SLOW SEEDLING GROWTH
We are now in a position to reconsider the question of what limits the
distribution and abundance of conifers and how angiosperms might be
implicated. If productivity is relevant to interspecific competition then one
would expect gymnosperms to be poor competitors as seedlings and juveniles but
superior competitors as adults (Fig. 3 ) . Many tree species establish in gaps
created by disturbances such as wind throw, fire and flooding or by the
senescence of canopy trees (White, 1979; Pickett & White, 1985). T h e environmental conditions encountered by seedlings in such gaps are very different from
those experienced by parents in the canopy. The weedy features of angiosperm
herbs and shrubs are particularly well suited to quick colonization and space
pre-emption in regeneration gaps wherever light, water and nutrients are
adequate for rapid vegetative growth. Gymnosperms, by contrast, are ill
equipped to survive the seedling stage if they have to compete with weedy forbs,
grasses or shrubs. Recruitment bottlenecks have been found to be important
constraints on adult distribution and abundance in plants and animals (Werner
1979; Werner & Gilliam, 1984; Goldberg, 1982, 1985; Grubb, 1977).
Gymnosperms, too, may be excluded from environments where their seedlings
encounter vigorous angiosperm competition-typically
sites with abundant
water, light and nutrients, and a long growing season.
W. J. BOND
238
ECOLOGY OF GYMNOSPERM DISlRIBUTIONS
Angiosperms can affect gymnosperms regenerating in gaps in at least four
specific ways. First, conifer seedling growth may be suppressed by angiosperms,
especially herbs, thereby prolonging the juvenile phase. The longer the seedling
remains suppressed, the more vulnerable it will be to death from drought, frost or
lethal temperatures (Chapman, 1945; Harper, 1977). Secondly competition at
the juvenile phase may prolong exposure of juvenile plants to destructive biotic
agents, including herbivores, pathogens and litterfall, when they are least
equipped to defend themselves (Vaartaja, 1962; Taher & Cooke, 1975; Grime,
1979). Thirdly, angiosperms may radically alter disturbance cycles so that slower
maturing gymnosperms would be eliminated. For example, fires may sweep
through grasslands killing juvenile conifers before they can overtop and suppress
the herbs (Wells, 1965). Finally, even with unchanged disturbance cycles, conifer
regeneration may be suppressed by quick-growing angiosperm herbs or shrubs,
and the conifers may fail to reach maturity before the stand is replaced following
another disturbance (Fig. 4).
I A
Time
Figure 4. Potential effects of angiosperms on gymnosperm growth and survival. Th e shaded area
represents the typical range of disturbance frequencies. T h e dashed line, RT, indicates a sizedependent reproductive threshold. ang = angiosperm competitors present; ang- = no effect from
angiosperms. A, No effect or1 disturbance; B, angiosperms alter disturbance frequency.
+
ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE
239
I n all four cases, angiosperm competitors are not directly responsible for the
demise of conifers but act through a “third party” (Grubb, 1985) such as drought,
fire or fungal pathogens. Thus a conifer seedling regenerating under a dense patch
of herbs may survive and slowly overtake its competitors unless some
environmental ‘challenge’ intervenes such as drought. However, as a first
generalization, the slow seedling hypothesis predicts that conifers should be
excluded from environments which support dense, rapid vegetative growth in
regenerating patches. They would persist best in sites where vegetative growth is
slow or where favourable conditions are too brief for dense swards to develop.
Conifers would therefore be least threatened by angiosperms in cold climates,
climates with a short growing season, or on nutrient poor soils where vegetative
growth is slow to close a regenerating gap. Conifers would also tend to be
excluded from communities with short intervals between disturbance, especially if
juvenile growth is retarded in any way by angiosperm competitors.
Biogeographic evidence
The global distribution of conifers seems to be compatible with the prediction
that they should occur where conditions for rapid vegetative growth are poorest.
Contemporary conifers persist in greatest numbers at high elevations or
latitudes-the
great northern boreal forests, and montane temperate and
tropical forests-where vegetative growth is limited by low insolation, cool
temperatures and short growing seasons (Schmithusen, 1960; Florin, 1960;
Fowells, 1965; Whitmore, 1975; Regal, 1977; Daubenmire, 1978). These regions
support low frequencies of growth forms indicative of the capacity of a site to
sustain rapid growth rates, such as deciduous plants and annual herbs (Bliss,
1971; Billings & Mooney, 1968; Cain, 1950; Table 3 ) . Deciduous arctic trees are
common only where water and nutrients are abundant during the growing
season (Chapin, 198 1 ; Heinselman, 1981a ) .
‘I’ABLE3. T h e incidence of annual herbs (therophytes) in relation to
altitude. Values arc annuals as a percent of all species in each area
(ex Cain, 1954)
Locality
Clova, Scotland
Poschiavo, Alps
Annuals
Altitude (m)
No. of species
1000+
900- 1000
800-900
700-800
600-700
500-600
400-500
300-400
< 300
11
44
72
170
206
182
193
21 1
304
0
7
4
4
5
4
4
5
13
2850 +
2550-2850
2250-2550
1900-2250
1550-1900
1200-1550
850-1 200
< 850
51
199
348
492
487
449
604
447
2
4
6
6
8
14
19
21
,(;(
240
W. J. BOND
Outside boreal and montane regions, conifers generally occur on nutrient poor
sites, especially sandy, acidic, or waterlogged soils. I n California, for example,
conifer ‘islands’ in chaparral and oak woodlands are associated with acid sands,
serpentines, diatomaceous earths etc. (Mason, 1946; McMillan, 1956; Gankin &
Major, 1964; Wells, 1962; Kruckeberg, 1969, 1985; Vogl, 1973). I n the southeastern United States conifers are also associated with sandy and nutrient poor
soils (Forman, 1979; Zobel, 1969). Tropical pines in the Americas and South-East
Asia occur on nutrient-deficient podsols quite distinct from rain-forest soils
(Whitmore, 1975; Kellman, 1984). I n Australia, Callitris and Actinostrobus
(Cupressaceae) form extensive woodlands on infertile sands (Lacey et al., 1982;
Page & Clifford, 1981) and in South Africa Widdringtonia (Cupressaceae) is
similarly restricted to low fertility heath sites (Kruger, 1977). Tropical lowland
conifers including Araucaria, Agathis, and Dacrydium typically occur on heathy sites
(kerangas) on infertile sands, acid bogs or occasionally on acid pockets of humus
on limestone (Whitmore, 1975; Whitmore & Page, 1983; Regal, 1977; 1982).
There is no evidence from either plantation forestry or experimental
transplants that edaphically restricted conifers prefer nutrient-poor soils. O n the
contrary, studies of Californian conifers restricted to infertile soils show that they
nearly always grow better on more fertile soils (McMillan, 1956; Griffin, 1965).
These results have led many authors to argue that edaphic endemism is
maintained by competition between mature conifers and more vigorous woody
species on richer soils (Kruckeberg, 1969, 1954; Gankin & Major, 1964; Grime,
1979). The problem, however, is that edaphically restricted conifers (e.g. Pinus
radiata, Pinus merkusii) are not primitive slow growing relicts but highly productive
species, some of which form the basis for a plantation forestry industry far beyond
their native range, and soon overtop their native competitors. Experimental
studies suggest that the basis for edaphic endemism may lie, instead, in release
from competitors in the regeneration niche. T h e vegetation of nutrient poor soils
is characterized by slow relative growth rates, slow foliage turnover and
perenniality (Beadle, 1954; Loveless, 1961; Monk, 1966; Specht, 1979; Chabot &
Hicks, 1982). Nutrient-poor soils therefore provide a refuge from competition for
slower growing seedlings, including those of conifers, because regenerating
patches close more slowly (see Goldberg, 1982, 1985 and Buckley, 1984 for
angiosperm examples).
Site productivity also influences the disturbance regime. Lacey et al. (1982)
suggest that Callitris columellaris (Cupressaceae) is restricted to poor sandy soils
because the sparser biomass of herbs on these sites does not carry fire as readily
as the better soils. Tree seedlings therefore have more time to become established
between fires (Lacey et al., 1982).
Experimental evidence- forestry and population studies
Although biogeographic patterns support the prediction that conifers are
restricted to sites which lack a competitive regeneration niche, Regal’s (1977,
1982) pollination hypothesis has similar predictions. He argues that
heterozygosity can only be maintained in dense stands of wind pollinated species
in low diversity communities and that low diversity is associated with climatic or
nutrient stress (Table 4).Experimental evidence is needed to test the separate
explanations for gymnosperm biogeography.
ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE
24 1
TABLE
4. Comparison of t h e pollination hypothesis and t h e slow seedling hypothesis for angiosperm
a d v a n t a g e and gymnosperm limitations
~
~~
Slow seedling
Morphological basis of
angiosperm advantage
Functional effect
Predicted gymnosperm range
Explanation of range
Assumed mechanism
Leaf and vascular anatomy, rate
of reproduction
Assimilation, productivity
Reproductive rates
‘Stressful’ environments e.g. cold,
nutrient-poor
Refugia for slow-growing juveniles
from fast-growing angiosperms
(a) Competition leading directly or
indirectly to increased mortality.
(b) Increased disturbance rates
eliminate slow-maturing
gymnosperms
Pollination
Flower/fruit, quality of
reproduction
Insect pollination
Seed dispersal by animals
‘Stressful’ environments e.g. cold,
nutrient-poor
Wind pollination requires dense
populations which occur in speciespoor communities. Low diversity is
caused by ‘stress’ conditions
Heterozygosity is correlated with
interspecific competitive ability.
Sparse wind-pollinated populations
are more homozygous than sparse
insect-pollinated populations
There are no experimental tests of the pollination hypothesis. T h e central
assumption that wind pollination is inefficient in species rich communities has
not been directly tested. There seems to be no data a t all, for example, on
pollination of sparsely distributed conifers such as Podocarpus scattered in the
broad-leaved southern hemisphere forests or Tuxus in the understory of northern
forests. I n the case of the slow seedling hypothesis, however, there is abundant
experimental evidence demonstrating the competitive effects of angiosperms on
gymnosperms. Conifers have been widely planted by foresters outside their
natural ranges. These experimental plantations have repeatedly demonstrated
startling capacities for tree growth and survival far beyond natural climatic
limits. For example, Pinus ponderosu plantations in the prairies of the Great Plains
survived the most severe drought on record and grew to 7 m in 30 years in the
arid ‘grassland’ climate (Wells, 1965). Evidently grasses both compete with tree
seedlings and carry fires that kill trees before they can overtop and suppress the
grasses (Wells, 1965). Conifers are excluded from the Great Plains less by the
‘grassland climate’ than by the effects of grasses on the disturbance cycle and on
regenerating tree seedlings (Wells, 1965; Axelrod, 1985).
Removal of understory competitors is a n important silvicultural treatment in
commercial forestry and has been repeatedly shown to have a major influence on
the establishment of many timber species (see references in Tourney & Keinholz,
1931; Fowells, 1965; Stewart, Gross & Honkala, 1984; Sands & Nambiar, 1984;
McDonald, 1986). Angiosperm competition with conifers causes either increased
seedling mortality, usually in the first year or two of establishment, or decreased
growth of saplings. Angiosperm herbs, especially grasses, outgrow and shade the
conifers and compete for water and nutrients in the surface layers of the soil (see
e.g. Shirley, 1945) (shading can also be beneficial in reducing lethal soil
temperatures). Conifers are excluded from many regions by grasses which
suppress the growth of tree seedlings (e.g. Pearson, 1942; Johnsen, 1962; Hadley,
1969; Burkhardt & Tisdale, 1976; Sims & Mueller-Dombois, 1968).
Although angiosperm competition in the regeneration niche is an important
component, the causes of these recruitment bottlenecks are usually complex and
242
W. J . BOND
multifactorial. For example, the origin of cohorts of similarly aged junipers in
rangelands can often be traced to episodes of' heavy grazing (which leads to
decreased competition between grass and tree seedlings), reduced fire frequencies
and higher than average precipitation or the coincidence of two or more of them
(Johnsen, 1962; Smith, Wright & Schuster, 1975; Madany & West, 1983). The
studies cited above refer mostly to seasonally arid woodlands or savannas, but
herbs can also severely inhibit seedling establishment after disturbance in other
environments, for example in mesic forests such as those of the Pacific Northwest
(Strothmann & Roy, 1984), alpine meadows where grasses and forbs inhibit the
invasion of coniferous trees (Franklin, Moir, Douglas & Wiberg, 1971; Kotar,
1978), or Mediterranean shrublands where grasses inhibit establishment of Pinus
halepensis seedlings (Acherar, Lepart & Debussche, 1984).
In addition to herbs, angiosperm shrubs and small trees are also important
competitors of juvenile conifers (Conrad & Radosevich, 1982; Hobbs &
Wearstler, 1985; McDonald, 1986). In the absence of disturbance, severe
droughts or the attack of herbivores or pathogens, suppressed conifers may
eventually survive to reach the canopy. For most North American conifers,
however, suppressed growth increased the risk of death from periodic drought
(Chapman, 1945), fire (Arend, 1950; Burkhardt & Tisdale, 1976; Strothman,
1967) or herbivory, especially by vertebrates. For example Chapman (1945), in a
study of Loblolly pine (P. taeda) regeneration, found that the shade of low
hardwood shrubs was fatal to pine seedlings. Under high overhead shade,
however, and in the absence of low shrubs Loblolly pine survived as suppressed
seedlings or saplings for up to 20 years, provided that no severe droughts
occurred. These suppressed saplings remained vulnerable to light surface fires at
any season whereas seedlings in open sunlight rapidly gained resistance to surface
fires. Similar examples occur wherever fire is important in initiating regeneration
(Strothmann & Roy, 1984; Wright & Bailey, 1982; Heinselman, 1981a, b).
Shade-tolerant conifers
The majority of gymnosperms regenerate in large openings created by
disturbances such as fire and windstorms (e.g. Fowells, 1965; Whitmore, 1975).
A few, however, are shade-tolerant and regenerate in openings created by a
single tree or branch fall (e.g. Tsuga canadensis, Podocarpus spp.). Indeed one
would expect gymnosperms to persist in such habitats since deep shade would
reduce the growth advantages of'angiosperms in the same way as nutrient poor
soils and cold climates. Though shade tolerant conifer seedlings do compete with
understory angiosperms for the most favourable space on the forest floor
(Maguire & Forman, 1983), many survive and persist for years as slow growing,
suppressed understory trees.
The principles underlying relative abundance and species diversity in forests
with tree by tree replacement are still poorly understood (Hubbell & Foster,
1986) but some studies suggest similar processes to those discussed above.
Gymnosperms have a more rigid architecture than angiosperm trees and have a
lower rate and propensity for reiterating branches (Brown, 1971; Halle,
Oldeman & Tomlinson, 1978). Consequently they may be less opportunistic at
filling space made available by the death of neighbours (e.g. Hibbs, 1982). Halle
et al. (1978) attribute the greater plasticity of angiosperm architecture to the
ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE
243
more efficient transport system of angiosperms coupled with larger, more
productive leaves.
If gymnosperms are less able to respond to sudden changes in the canopy
environment due to the death of neighbours, then (a) gymnosperm canopy trees
will be slower than angiosperms to fill gaps in the forest by lateral growth and
(b) gymnosperm saplings will be slower than angiosperm saplings to fill gaps in
the canopy by height growth. Hibbs (1982) has provided quantitative data for a
north temperate hemlock-hardwood forest. He showed that lateral growth of
Tsuga canadensis, a conifer, was the slowest of the five tree species he measured
(the rest all angiosperms) while height growth of hemlock saplings in small gaps
was also by far the slowest (Hibbs, 1982; see also Runkle & Yetter, 1987). Ifsuch
patterns prove general, then shade-tolerant gymnosperms would be restricted to
forests where (a) growth rates are slow because of climatic or nutrient limitations
on productivity, (b) gaps are small and saplings are shaded and ( c ) there are
very long intervals between major stand-destroying disturbances so that the slow
growing conifers have sufficient time to reach the canopy. These predictions
differ from Regal’s (1977) suggestion that gymnosperms should be confined to
“low diversity” forests. Species richness would not be an important factor in
gymnosperm distribution. However gymnosperms should be excluded from
forests with dense liana growth, a high frequency of compound leaves or other
structural attributes indicative of rapid secondary growth or rapid filling of
canopy gaps. There are too few studies to test these predictions for shade-tolerant
conifers but this is currently a n active area of research (see reviews in Pickett &
White, 1985).
DISCUSSION
The central question I attempt to answer is: what restricts modern
gymnosperm distribution? Despite the high productivity of mature conifers, the
growth rates of juveniles are low. I argue that competition from angiosperms in
the regeneration niche is currently the most plausible hypothesis for the many
gymnosperms which regenerate after disturbance. T h e main competing
hypothesis is that gymnosperms are limited by the inherent limitations of wind
pollination to living in relatively pure stands (P. Raven, 1977; Regal, 1977,
1982; Burger, 1981). Both hypotheses are general-that
is they assume a link
between functional morphology, ecology and the distribution of major taxa
(Table 4).Almost no direct evidence exists to test the pollination hypothesis SO
that its breadth of application is unknown. The slow seedling hypothesis,
however, is supported by considerable experimental evidence for the importance
of angiosperm competition in gymnosperm regeneration and rather less evidence
for lethal effects of angiosperms on the disturbance regime. I n the case of shadetolerant gymnosperms (which escape competition as seedlings) populations
appear to be limited, by the same growth constraints, to forests with small gap
sizes and very infi-equent large-scale disturbances.
T h e regeneration niche and the fossil record
Does the slow seedling hypothesis explain Cretaceous extinctions of
gymnosperms? There are many difficulties in determining process from pattern in
the paleobotanical record and the patterns themselves are still controversial
244
W. J BOND
(Knoll & Rothwell, 1981; Knoll, 1986; Hickey & Doyle, 1977; Krassilov, 1978).
Current interpretations of the fossil record suggest that the angiosperm invasion
began from small shrubs in semiarid (Stebbins, 1974) or seasonally dry (Hickey &
Doyle, 1977) tropical highlands. T h e weedy attributes of angiosperms were the
basis of their initial rapid spread into a variety of unstable depositional
environments such as fluvial and deltaic levees and tidal flats (Doyle & Hickey,
1976, Hickey & Doyle, 1977). These temporary habitats were common
worldwide because of the breakup of continents and marine transgressions
(Retallack & Dilcher, 1981; Frakes 1979). Later, angiosperms diversified into a
variety of niches and they began to enter the understory of coniferous forest in
more stable landscapes (Doyle & Hickey, 1976; Doyle, 1977; Krassilov, 1978).
The first angiosperm trees to reach the canopy only appeared in the beginning of
the Late Cretaceous (Doyle, 1977). Indeed some authors have argued that
conifers continued to dominate forest canopies until the very end of the
Cretaceous with angiosperms merely filling the once-empty understory (Doyle,
1977; Krassilov, 1978).
The distinction between enrichment of gymnosperm paleofloras by
angiosperms occupying new niches or the replacement of gymnosperms by
vigorous angiosperm competitors is often ignored in discussions of the basis of the
angiosperm success. Yet the timing of gymnosperm decline is crucial to some
explanations, particularly those which invoke coevolution with animal
pollinators, dispersers or herbivores ($ Regal, 1977; P. Raven, 1977). Thus
Regal (1977) argued that the dispersal of angiosperm seeds by birds was
important in early angiosperm radiation yet abiotic dispersal predominated
throughout the Cretaceous (Tiffney, 1984). With these uncertainties it seems
futile to argue for a single cause of gymnosperm decline. For example, Krassilov
(1 978) has suggested that a terminal Cretaceous catastrophe caused the
extinction of the Mesozoic conifer overstory. However a catastrophist hypothesis
cannot explain the demise of the Cheirolepidiaceae in the mid-Cretaceous nor the
relative increase in conifer pollen immediately above the Cretaceous-Tertiary
boundary (Saito, Yamanoi & Kaiho, 1986).
It is often assumed that direct competition between angiosperms and
gymnosperms only commenced when angiosperms evolved canopy trees, that is,
when the adult growth forms closely overlapped. The potential importance of
angiosperms slowly intruding into the juvenile niche of gymnosperms has been
overlooked. Competition between angiosperm shrubs and regenerating trees
would have existed early in the Cretaceous with the most severe consequences in
regions with periodic drought-such
as the seasonal tropics where the
Cheirolepidiaceae were the first of the gymnosperms to go extinct (Alvin, 1982).
The modern interaction between competition and disturbance cycles could also
have occurred early in angiosperm evolution. Early angiosperms were associated
with the most frequently disturbed terrain in Cretaceous floodplains (Doyle,
1977; Retallack & Dilcher, 1981) and fires swept through Mesozoic forests
creating favourable conditions for weedy, early successional angiosperms (Harris,
1958). Dinosaurs may even have created opportunities for weedy angiosperms as
they blundered through Cretaceous conifer forests (Wing & Tiffney, 1987).
However, although herbs evolved very early in the Cretaceous (Doyle & Hickey,
1976), grasses only become important in the Oligocene and their effects on
conifers may have occurred only as late as the Pleistocene (Axelrod, 1985).
ANGIOSPERM DOMINANCE AND GYMNOSPERM PERSISTENCE
245
CONCLUSIONS
Gymnosperms, and conifers in particular, are an excellent case-study in the
search for generalizations linking functional morphology with ecology. The
hypotheses presented here suggest an envelope of possibilities within which
gymnosperms can co-occur with angiosperms. Whether they do occur within
these bounds depends on many other factors, the random accidents of dispersal,
the presence of a particular seed predator, fungal pathogens and their insect
vectors and so on. This attempt at a general explanation for the decline of
gymnosperms is justified by the perspective it gives to plant evolution. IS, indeed,
the giant sequoias retreated because of low weeds interspersed in their
understory then the circumstances that change the vegetation of the earth are
seen in a rather different light.
ACKNOWLEDGEMENTS
I benefitted from discussions with P. Grubb, A. Gibson, A. Knoll, P. Nobel, B.
Prigge, P. Regal and D. Walker amongst many others while developing these
ideas. M. Cody, P. Frost, L. Kohorn, F. Kruger, J. Midgley and P. Rundel made
useful comments on the manuscript. An anonymous reviewer pointed out some of
the pitfalls awaiting neontologists interested in paleobotany. The research was
supported by a Vavra and University of California Research Fellowship.
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