7
Temperate and Tropical
Podocarps: How Ecologically
Alike Are They?
David A. Coomes and
Peter J. Bellingham
ABSTRACT. With few exceptions, podocarps are specialists of nutrient-poor soils
within temperate and tropical rainforests. They are locally abundant in some tropical
mountains, especially near the tree line, and in the lowland tropics most are confined to
heathlands and impoverished habitats, although some can persist in forest understories.
The ecology of tropical podocarps is not well understood, so here we draw on literature
from temperate regions to help characterize their niches. Temperate podocarps are effective at capturing and retaining nutrients at the expense of competitors. They are universally slow growing, but this is not necessarily an encumbrance on poor soils because
competition for light is relatively weak. Temperate podocarps are often outcompeted on
richer soils because several factors stack against them: they are ill equipped to compete
with angiosperms in the race to occupy canopy gaps, there may be few sites for their
establishment on the forest floors, and continuous regeneration by podocarps is seldom
found in the forest understory because their growth is severely hampered by shading. We
suggest that competition excludes imbricate-leaved podocarps from most lowland tropical forests, whereas broad-leaved species with anastomosing veins (Nageia and some
Podocarpus) are so shade tolerant that they regenerate beneath closed canopies.
INTRODUCTION
David A. Coomes, Forest Conservation and
Ecology Group, Department of Plant Sciences,
University of Cambridge, Cambridge CB2 3EA,
UK. Peter J. Bellingham, Landcare Research, PO
Box 40, Lincoln 7640, New Zealand. Correspondence: David A. Coomes, dac18@cam.ac.uk.
Manuscipt received 13 April 2010; accepted
9 July 2010.
In 1989, Bond revisited an old but unresolved question: why were conifers pushed out of the lowland tropics and mesic temperate regions by angiosperms as they diversified and expanded in range during the Late Cretaceous?
Previously, the leading hypothesis was that the evolution of flowers had given
angiosperms overwhelming reproductive superiority over conifers: the wasteful process of wind pollination was usurped by directed pollination by animals
(Raven, 1977). Bond (1989) and Midgley and Bond (1991) challenged the prevailing view, hypothesizing instead that the physiological traits of conifers made
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them inherently slow growing as seedlings. These traits
place them at a competitive disadvantage during the regeneration phase of the life cycle but help them survive in
extreme environments, including cold, droughts, nutrientpoor soils, poorly drained soils, and deep shade.
Two decades after Bond’s “slow seedling” hypothesis,
the latest physiological evidence indicates that podocarps
are universally slow growing. Podocarps have long-lived
leaves and low specific leaf areas, traits always associated with low photosynthetic capacity per unit leaf mass
(Wright et al., 2004). They have lower photosynthetic capacity than angiosperms of comparable specific leaf area
(Lusk, this volume). Using a global database of wood densities, we find that podocarps have denser wood than other
conifers (Figure 7.1); this trait is associated with podocarps having narrower tracheids (Pittermann et al., 2006a;
Lusk, this volume) and results in high hydraulic resistivity
and low photosynthetic capacity per unit leaf area (Feild
and Brodribb, 2001). In lowland cool temperate forests,
diameter growth of podocarp trees is approximately half
that of angiosperm trees under similar conditions (Ogden
and Stewart, 1995; Bentley, 2007). In subalpine shrublands, podocarps grow more slowly than several angiosperms (P. Wardle, 1963a). Podocarps are slower growing
than other commercially valuable timber species (Bergin,
2000). For example, Podocarpus totara seedlings with
an initial mean height of 0.85 m reached just 2.9 m after 6 years and 5.5 m after 11 years in a provenance trial
on fertile soils under frost-free conditions (Bergin et al.,
2008), whereas Pinus radiata reaches heights up to 30 m
after 17 years (Beets and Kimberley, 1993). Seedlings of
Lagarostrobos franklinii in Tasmania grow at just 2.3 cm
yr-1, approximately a third of the rate of the angiosperm
tree Eucryphia milliganii, which grows in nearby forests
(Jennings et al., 2005). Podocarp seedlings are outpaced
by angiosperms and even by tree ferns when growing on
rich soils in southern New Zealand: height growth under
optimal conditions is 3–7 cm yr-1 versus 11–17 cm yr-1
for subcanopy angiosperms and ~10 cm yr-1 for tree ferns
(Gaxiola et al., 2008; Coomes et al., 2009). We found no
examples of fast-growing podocarps.
The notion that conifers are well equipped to cope
with extreme environments remains unchallenged, but the
mechanisms by which conifers are competitively disadvantaged in “productive” habitats are still a topic of debate.
In the case of podocarps, there is considerable doubt over
whether they can even be described as disadvantaged in
lowland tropical habitats since a considerable number of
shade-tolerant podocarps grow in the shade of tropical
forests (e.g., Hill and Brodribb, 1999). The ~30 species of
FIGURE 7.1. Wood density (oven-dry mass/fresh volume) of
podocarp species from temperate and tropical regions (extracted
from a global database; Chave et al., 2009). The Podocarpaceae
have a greater mean wood density than six other conifer families (0.50 g cm-3 vs. mean of 0.45 g cm-3; F7,260 = 9.7, P < 0.001)
and a similar mean density to the Taxaceae (0.53 g cm-3).
Tropical podocarps have a significantly lower wood density than
their temperate relatives (0.48 ± 0.01 vs. 0.54 ± 0.02 g cm-3; t = 2.1,
P = 0.03).
podocarps found in cool temperate forests have received
much more attention from ecologists than the ~150 species of tropical and warm temperate forests. Can our understanding of the ecology of these temperate podocarps
inform us about the distribution and dynamics of their
tropical cousins? We start by discussing what types of
habitats are occupied by temperate podocarps and why
they are not observed in the full range of high-stress habitats occupied by conifers as a whole. We then explore the
reasons why temperate podocarps often achieve dominance on nutrient-poor soils and why the exceptions prove
the rule. We look at the regeneration strategies of temperate podocarps in shaded habitats and how these help
explain the presence and persistence of some species in
more nutrient-rich forests. These analyses lead us back to
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a discussion of the ecology of tropical podocarps and why
they are relatively uncommon in the lowlands.
LIMITS TO GEOGRAPHIC DISTRIBUTION:
INTOLERANCE OF COLD AND DROUGHT
Podocarps prevail mostly in climates that are cool
and wet. However, they do not tolerate extreme cold as
well as Northern Hemisphere conifers: none can withstand temperatures below -20°C, whereas 88% of 117
Northern Hemisphere conifer species can do so (Figure
7.2; Bannister, 2007). Podocarps seldom form the tree line
in temperate mountains but do so in tropical mountains.
Instead, Nothofagus species often form tree lines in cool
temperate South America, New Zealand, and Tasmania;
podocarps are present but seldom form significant components of these forests (Wardle, 2008). Some temperate
podocarps occur almost exclusively above tree lines as
shrubs or prostrate woody plants in alpine ecosystems in
New Zealand (Wardle, 1991) and Tasmania (Kirkpatrick,
1997). Perhaps differences in present and past climate
have reduced the need and opportunity for the evolution
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of traits conferring tolerance of extreme cold. Southern
Hemisphere oceans act as vast heat buffers that moderate land temperatures, resulting in milder climates than
in the Northern Hemisphere. The Southern Hemisphere
was also less extensively glaciated during the Pleistocene
(Sakai et al., 1981). Mild climates throughout much of
the evolutionary history of the Southern Hemisphere may
be responsible for its paucity of cold-tolerant trees: New
Zealand’s tree lines, at 1,200–1,300 m, are about 500 m
lower than continental tree lines at equivalent continental
latitudes (Körner and Paulsen, 2004).
Although podocarps are ill equipped to survive in extreme cold, they are relatively well protected against moderate frosts experienced in their current ranges. Frosts in
New Zealand’s North Island damage the dominant shadetolerant angiosperm (Beilschmiedia tawa) but have no
apparent effect on co-occurring podocarps (Kelly, 1987).
Pot-grown podocarp seedlings are more tolerant of subzero temperatures than angiosperms taken from the same
region (Bannister and Lord, 2006). Hardiness of Podocarpus totara in New Zealand has a strong genetic basis,
with genotypes from the coldest regions being most hardy,
suggesting that populations have evolved in response to
FIGURE 7.2. Frost resistance of conifers from the Northern (light gray) and Southern
(dark gray) hemispheres, redrawn from Bannister (2007). Frost resistance was quantified by calculating the temperature at which half of the leaves are damaged by the
effects of cold.
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environmental pressures (Hawkins et al., 1991). Their
frost hardiness appears to come at a cost, in that maximum
growth rates of high-latitude genotypes are slower (Bergin
et al., 2008). Angiosperms in Tasmanian montane heaths
suffer much greater loss in xylem conductivity after being
frozen and thawed (17%–83%) than do conifers (<12%),
primarily, it seems, because bubbles in the xylem conduits
formed during the freeze-thaw cycle are more easily redissolved in the narrow tracheids of conifers than in the wider
vessels of angiosperms (Feild and Brodribb, 2001).
Few temperate podocarps grow in dry regions, in contrast to other conifers, and this intolerance can be traced
to their vascular systems (see also Brodbribb, this volume).
Exceptions include Afrocarpus falcatus in drier regions of
southern Africa (Adie and Lawes, this volume), Podocarpus drouynianus in Western Australia (Ladd and Enright,
this volume), and Halocarpus bidwillii, Phyllocladus alpinus, and Podocarpus hallii in the dry lowland forests
of New Zealand (~400 mm yr-1; Bergin, 2000; McGlone,
2001). Drought damages plants if the tension within water columns of the vascular system gets so large (i.e., the
water potential gets so low) that cavitation occurs or if
conduits implode (Tyree and Sperry, 1989). Plants from
dry regions, such as conifers in the Pinaceae and Cupressaceae, withstand high tensions within their vascular systems by having thick tracheid walls that prevent implosion
and “plugs” (torus margo) within pit membranes that prevent air bubbles from moving through the vascular system (Pittermann et al., 2006b). However, podocarps are
peculiar among conifers in being susceptible to embolism
at relatively low tensions, despite having thick tracheid
walls (Pittermann et al., 2006b) and having relatively high
hydraulic resistance across pit membranes (Pittermann et
al., 2006a). It may also be the case that sclereids in podocarp leaves are vulnerable to implosion under tension
(Brodribb, this volume). Plants can avoid damage by early
closure of stomata, but we found no studies of stomatal
responses in podocarps. Podocarps have long-lived leaves,
so they are unable to drop all their leaves during dry periods in the way that many drought-deciduous angiosperms
do. In one example, Podocarpus totara lost many leaves
during a drought year, produced shorter leaves, and maintained high internal water potential but fared less well than
drought-tolerant angiosperms (Innes and Kelly, 1992).
TOLERANCE OF NUTRIENT-POOR SOILS
With a few important exceptions, podocarps in the
cool temperate regions achieve greatest abundance on the
poorer soils and/or in open habitats. In the coastal range of
Chile, two podocarps are most common on shallow mica
schists and poorly drained sites (Lusk, 1996), and Lepidothamnus fonkii has a dwarf habit and grows in Sphagnum
bogs (Gardner et al., 2006). In Japan, Nageia nagi occurs
on thin soils derived from granite on Yakushima (Kohyama
and Grubb, 1994), but it is not restricted to poor soils. In
southeastern Australia, Podocarpus lawrencei occurs on
acidic soils on granite and weathered sedimentary rocks,
achieving greatest abundance on skeletal soils (Barker,
1991). In New Zealand, podocarps often achieve greatest
abundance on poor soils, as shown by investigations on
two soil chronosequences: a series of deglaciated terraces
near the Franz Josef Glacier and a series of uplifted marine
terraces in southern Fiordland. On both chronosequences,
plant-available phosphorus becomes depleted on the
older sites, and podocarps become increasingly abundant
on these impoverished soils, with some species restricted
to them (Richardson et al., 2004; Coomes et al., 2005).
Bond (1989) proposed that conifers are successful on poor
soils because they are almost unrivalled in their tolerance
of extreme environments and because competition for
resources is neither intense nor important; conifers are
stereotyped as “stress tolerators” in the competitor–stress
tolerator–ruderal triangle of Grime (1977). Here we argue
that podocarps possess traits that allow them not only to
tolerate poor soils but also to be successful competitors for
belowground resources.
EFFICIENT CAPTURE OF NUTRIENTS
Fungal hyphae have high area to mass ratios, making them more efficient than roots at foraging for immobile nutrients. Podocarps rely heavily on endomycorrhizal
symbionts for nutrient uptake (Baylis, 1969; Russell et al.,
2002). Fine roots have low specific root length (Gaxiola et
al., 2010) and are heavily infected by mycorrhizal fungi (up
to nearly 100% of root length; Dickie and Holdaway, this
volume). Podocarps on the Franz Josef chronosequence
had lower foliar nitrogen to phosphorus ratios than ferns
or angiosperms on the phosphorus-impoverished soils,
suggesting that they were better able to extract soil phosphorus (Richardson et al., 2005). Angiosperm species
from podocarp-rich forests are also heavily infected by arbuscular mycorrhizas (Hurst et al., 2002), but very little is
known about the comparative efficiency of these groups.
Slow-growing conifers from the Northern Hemisphere allocate a large proportion of their net primary productivity
to roots and ectomycorrhizal fungi, particularly when nutrients are in short supply (Hobbie, 2006). The same may
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be true of podocarps: Whitehead et al. (2004) concluded
that Dacrydium cupressinum in New Zealand swamp
forests allocate a high proportion of total carbon belowground, on the basis of the predictions of a process-based
simulation model. New Zealand podocarp seedlings have
a higher root to shoot ratio that many angiosperm trees,
particularly when grown in nutrient-poor soils.
INCREASED NUTRIENT RETENTION OF LONG-LIVED LEAVES
Species associated with nutrient-poor soils often have
long-lived leaves (Grime, 1977; Chapin, 1980; McGlone
et al., 2004) because a long life span reduces the annual
rate of mineral nutrient loss via abscission (Monk, 1966).
Plants salvage only about 50% of nitrogen and 60% of
phosphorus from leaves during abscission (although there
is great variability among species), so retaining leaves is
strongly advantageous in situations where recapturing nutrients is costly (Aerts, 1995). Podocarp leaves have long
life spans compared with angiosperm associates; Gaxiola (2006) observed that four podocarps species from the
Waitutu chronosequence in southern New Zealand had a
mean leaf life span of 3.1 years, compared with 1.5 years
for 11 angiosperm species (nine of which were evergreen).
Lusk (2001) measured leaf life spans of several Chilean
species, including the following podocarps: Podocarpus
nubigenus (7.3 years), Podocarpus salignus (3.2 years),
and Saxegothaea conspicua (4.2 years). Podocarp leaves
contain significant quantities of terpenes (Brophy et al.,
2000), which are known to deter herbivores. However,
whether podocarps are better defended than angiosperm
is difficult to judge objectively because terpenes are just
one of the armory of defenses that plants deploy.
LONGEVITY AND NUTRIENT RETENTION
Some temperate conifers, including podocarps, have
much longer life spans than co-occurring angiosperm trees
(Wardle, 1991; Enright and Ogden, 1995). This is especially the case for some New Zealand podocarps (Lusk and
Ogden, 1992; Bentley, 2007) and Lagarostrobos franklinii
in Tasmania (Gibson and Brown, 1991). However, great
longevity is not a feature of podocarps, whereas it is of
other conifers in the same forests (e.g., Cryptomeria japonica and Tsuga sieboldii in Japan, Fitzroya cupressoides
in Chile, and Picea balfouriana in China). A tree releases
nutrients back to the soil upon its death, so a long life span
is advantageous in situations where regaining those nutrients requires intense competition with neighbors (Ogden
and Stewart, 1995; Coomes et al., 2005). A long life span
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requires wood that is strong and resistant to boring insects
and rot. Podocarps have denser wood than other conifers
(Figure 7.1), indicating that the wood is likely to be mechanically strong (Chave et al., 2009). Many podocarp
species are prized for their timbers because they are resistant to rot, and powerful antimicrobial chemicals have
been isolated from the bark of several Podocarpus species
(Abdillahi et al., 2008). An array of diterpenoids within
bark (Cox et al., 2007), as well as the deposition of phenolics in specialized parenchyma cells (Hudgins et al., 2004),
provides robust defense against insects.
ECOSYSTEM ENGINEERS THAT STARVE
NEIGHBORS OF NUTRIENTS
The tough fibrous leaves of New Zealand’s podocarps are slow to decompose (Wardle et al., 2008; Hoorens et al., 2010), resulting in the accumulation of organic
matter within soils, an increase in the ratios of carbon to
phosphorus and nitrogen to phosphorus in soil, and effects on community structure of soil microflora (Wardle
et al., 2008). Nutrients are sequestered within the recalcitrant organic matter. Locking up nutrients in this way is
an effective means of competing for nutrients if competitors are relatively intolerant of extreme nutrient shortage
or less able to access organic nutrients. In effect, podocarps may engineer their local environment to their own
advantage.
TOLERATORS OF SOIL ANOXIA
Nutrient-poor soils in high rainfall regions are often
poorly drained as a result of subsoil cementation. Species that tolerate low concentrations of soil oxygen and
mobilization of toxic ions are advantaged under these
conditions. A pot experiment with three New Zealand
podocarps showed them to survive well, with much reduced growth, under waterlogged conditions (Gaxiola et
al., 2010). The prevalence of conifers in waterlogged sites,
both in New Zealand and in other temperate forests, appears to result from various morphological and biochemical adaptations (Crawford, 1987). One New Zealand
podocarp, Manoao colensoi, produces aerenchyma in its
roots that carries air down to submerged fine roots (Molloy, 1995), but no other examples of this in podocarps are
known. The reduced stature of podocarps associated with
bogs (e.g., Lepidothamnus intermedius and Halocarpus
biformis in New Zealand) may result from a lack of deep
anchoring roots in anoxic soils, without which woody
plants are unable to grow tall (Crawford et al., 2003).
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REDUCED IMPACT FROM ASYMMETRIC
COMPETITION FOR LIGHT
CANOPY ARCHITECTURE SUITED TO
GROWTH IN THE OPEN
Podocarps are slow growing, which is not necessarily disadvantageous on poor soils, where resource limitations reduce the potential for fast growth regardless
of a species’ genetic potential. Forests on nutrient poor
and waterlogged soils often have comparatively low leaf
area indices and intercept less light (Coomes and Grubb,
2000). For example, 1.5% of incoming photosynthetically active radiation makes its way to the forest floor
of phosphorus-rich soils in southern New Zealand, 4.6%
gets through on phosphorus-depleted soils, and 16%
gets through on even poorer sites (Coomes et al., 2005).
The growth of podocarps is hardly influenced by competition from taller neighbors on the poor soils (e.g., Figure 7.3a). As long as competition for light is not intense,
podocarps may exclude other plants from nutrient-poor
soils through belowground competition (see Coomes and
Grubb, 2000).
Genera of podocarps associated with poor soils often have small, scalelike leaves held on upright or pendent stems (Dacrydium, Halocarpus, Lepidothamnus,
Manoao, Microcachrys, and Microstrobos) or have
whorls of leaves that overlap. Steeply inclined or clustered leaves reduce light interception at the top of the
canopy, allowing light to “trickle down” to lower leaves.
This increases whole-plant photosynthesis because the
uppermost leaves receive near-optimal rather than excessive light levels, while leaves at the bottom of the canopy
get a greater share of resources (Horn, 1971). The world’s
fastest-growing trees (Betula, Casuarina, and some Pinus
and Eucalyptus) have this canopy architecture, at least
once past the seedling stage. However, clumped and pendent leaves are inefficient at scavenging light in deeply
shaded understories and ineffective when competing for
light against fast-growing neighbors (Leverenz et al.,
FIGURE 7.3. Height growth of podocarp (dashed line) and angiosperm (solid line) tree seedlings in response to light on (a) phosphorus-depleted terraces versus (b) alluvial terraces in southern New Zealand.
The gray bars indicate the percentage daylight typically found at 1.35 m above ground under the canopy,
based on the 20th and 80th percentiles of light measurements (redrawn from Coomes et al., 2009).
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2000; Pickup et al., 2005). Therefore, these architectures
are uncommon in infrequently disturbed communities
growing on nutrient-rich soils where competition for light
is intense (Horn, 1971).
EFFICIENT USE OF LIGHT
The efficient use of whole-canopy light has been investigated in detail for Dacrydium cupressinum, which
has scalelike leaves positioned on pendent shoots; closed
stands have a leaf area index of only 2.0 m2 m-2 and intercept only 79% of available photosynthetically active
radiation when growing on acidic, poorly drained soil
(Whitehead et al., 2002). Clumping of leaves within the
canopy of Dacrydium-dominated forest reduces canopy
light interception by 5% but increases canopy photosynthesis by 8% through increased light use efficiency (Walcroft et al., 2005). Even though leaves in the upper crown
of Dacrydium on poor soils have a maximum rate of carboxylation activity (half-surface leaf area basis) that is
only 24% of that of similarly positioned leaves within an
oak woodland on nitrogen-enriched soils in summer, the
annual carbon uptake rate of the podocarp forest was only
14% lower than that of oak because of its canopy organization (Whitehead et al., 2004). The canopy architecture
and evergreen leaves, which continued to take up carbon
in winter, contributed to a higher-than-expected carbon
uptake rate.
SUMMARY
Podocarps are successful on poor soils because they
are well adapted to acquiring and retaining nutrients. It
may be that podocarps function similarly to slow-growing
conifers from the Northern Hemisphere, allocating a large
percentage of net primary productivity belowground and
thereby enabling their roots systems (and associated mycorrhizas) to forage exhaustively for soil nutrients. In addition, their long-lived leaves, durable wood, and slowly
decomposing litter ensure that hard-earned nutrients are
not relinquished to competitors. Inherently slow stem
growth may not be a serious encumbrance when nutrients are in short supply because asymmetric competition
for light is weak, so outgrowing neighbors is not strongly
advantageous. Any disadvantages that accrue from slow
growth are offset by effective nutrient recovery and retention, longevity, and strength to resist catastrophic disturbance. Scalelike leaves are advantageous in terms of
whole-plant photosynthesis in open habitats.
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REGENERATION PROCESSES
RESPONSES TO FOREST DISTURBANCE
Much attention has been given to the role of disturbances in allowing species with differing regeneration
niches to coexist within forests (Poorter and Bongers,
2006). In the context of Southern Hemisphere conifers,
Ogden and Stewart (1995) recognized three categories of
regeneration response to disturbance: (1) “Catastrophic
regeneration” occurs in the aftermath of infrequent massive disturbances (e.g., earthquakes, floods, fires, and
cyclones) and is characterized by a pulse of establishment after which no further establishment is possible; at
the landscape scale, catastrophic regeneration gives rise
to large patches (>1,000 m2) of similarly aged trees and
strong discontinuities in age structure within and among
patches. (2) “Gap-phase regeneration” occurs in smaller
gaps (<1,000 m2) created by the death a single tree or a
few trees; it is characterized by smaller patches and fewer
discontinuities in age. (3) “Continuous regeneration” occurs when seedlings and saplings are capable of growing
and surviving in the shade of an intact canopy. Typically,
these shade-tolerant trees edge slowly upward in the shade,
growing more quickly if openings appear in the canopy
above them (e.g., Uhl et al., 1988); near-continuous regeneration gives rise to all-aged population structures, composed of many small stems and successively fewer stem in
larger age classes.
Temperate podocarps vary greatly in shade tolerance.
Some have developed flattened leaves arranged within
planes, a shade adaptation that may have arisen in response to changes in light transmissions brought about by
the evolution of shade-bearing angiosperms in the early
Cenozoic (Hill and Brodribb, 1999; Brodribb and Hill,
2003a, 2003b). Podocarps with shade-tolerant leaf morphology also have shade-tolerant physiology (Brodribb,
this volume) and are sometimes capable of continuous regeneration. For example, Nageia nagi has large, flattened
leaves and regenerates nearly continuously within Japanese
warm temperate rainforests (Kohyama, 1986), and Prumnopitys ferruginea has shade-tolerant morphology and is
quite capable of establishing without multiple-tree gaps in
New Zealand (Figure 7.4; Duncan, 1993; Lusk and Smith,
1998; Bentley, 2007). Other species have tiny, scalelike
leaves held on upright stems and are unable to tolerate prolonged shade: when adult, Halocarpus biformis, a small
tree with imbricate scale leaves, is most frequent in open
habitats, such as the margins of bogs (Figure 7.4).
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FIGURE 7.4. Juvenile and adult foliage of contrasting podocarps from New Zealand. Drawings modified from
Wilson (1982) and reproduced with kind permission of the author and publisher.
REGENERATION PROCESSES IN
RELATION TO SOIL FERTILITY
Regeneration response depends not only on a species’ inherent shade tolerance but also on the light conditions in the understory of the forest. A species capable
of regenerating continuously under open forests on poor
soils may struggle to regenerate under dense forests on
richer soils. For example, two podocarps that grow in the
Chilean coastal range, Podocarpus nubigenus and Saxegothaea conspicua, are considered the most shade tolerant of all conifers in temperate South America (Donoso,
1989). They attain greatest abundance on shallow soils
(poorly drained sites in the lowlands, ridges, and shallow
mica schist at higher altitudes). The main angiosperms at
these sites (Nothofagus nitida and Weinmannia trichosperma) have open canopies under which the podocarps
regenerate: there are many seedlings and saplings in the
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forest understory, and the tree populations have reverse-J
age distributions (Lusk, 1996; Gutiérrez et al., 2004).
However, at sites where shade-casting angiosperms such
as Dasyphyllum diacanthoides and Laureliopsis philippiana are common, the podocarps are less abundant and
regeneration discontinuous (Lusk, 1996). At sites where
shade-tolerant angiosperms are dominant, the podocarps
are excluded altogether (e.g., Armesto and Fuentes, 1988).
In Tasmania, Lagarostrobos franklinii appears to regenerate along rivers that frequently flood but rarely penetrates
into closed rainforest (Gibson and Brown, 1991). In South
Africa, Podocarpus latifolius grows and survives well in
the understory of angiosperm-dominated warm temperate
forest in the Drakensberg Mountains (5.5% light transmission to forest floor; Adie and Lawes, 2009a) but is
unable to regenerate beneath coastal subtropical forest in
KwaZulu-Natal, through which only ~1% light is transmitted (Adie and Lawes, 2009b). However, the regeneration success of P. latifolius is not simply determined by
competition for light: seedlings are unable to establish under mature podocarp forest, even though 7.5% light penetrates to the forest floor, apparently because grasses and/
or mature trees exclude seedlings by belowground competition (Adie and Lawes, 2009a). Various other studies
indicate that that temperate podocarps fail to regenerate
beneath parent trees (e.g., Norton, 1991; Cameron, 1960;
Ogden and Stewart, 1995).
WHY SHADE-TOLERANT PODOCARPS FAIL
TO REGENERATE IN THE SHADE
Many podocarps persist in deep shade (e.g., mortality
rates in New Zealand lowland forest were just 1% per
year; Smale and Kimberley, 1986), but survival counts
for little unless accompanied by height growth. Height
growth of New Zealand podocarps is strongly suppressed
by shading (e.g., Smale and Kimberley, 1986; Ebbett and
Ogden, 1998; Coomes et al., 2009; Figure 7.3), limiting
opportunities for continuous regeneration in forest understories. For instance, Podocarpus hallii seedlings in a
cool montane rainforest in New Zealand have an annual
mortality rate of just 2.7%, meaning that about 5% of
seedlings live for at least 100 years, but height growth is
so slow that virtually no individuals get past the seedling
stage in the shade; consequently, most regeneration is restricted to landslides (Bellingham and Richardson, 2006).
Similarly, Dacrydium cupressinum seedlings had an annual mortality rate of 10% and a height growth of 1.5–
2.5 cm yr-1 in a lowland New Zealand forest on highly
leached soils, indicating that height growth is insufficient
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for seedlings to regenerate continuously in these forests
(Coomes et al., 2009; Kunstler et al., 2009). Instead, Dacrydium cupressinum requires progressive overstory mortality (Six Dijkstra et al., 1985; Lusk and Ogden, 1992;
Lusk and Smith, 1998; Bentley, 2007) or catastrophic disturbance (e.g., Duncan, 1993; Smale et al., 1997) in order
to regenerate. Even highly shade-tolerant podocarps such
as Prumnopitys ferruginea can struggle to get beyond the
seedling stage in lowland forests (Smale et al., 1997), and
stands of this species have a discontinuous age structure
at some sites (e.g., Lusk and Ogden, 1992). The important implication is that shade tolerance assessed from leaf
physiology does not necessarily equate with ability to regenerate continuously within a particular habitat. The latter depends upon the degree of shade cast by the forest as
well as the physiological shade tolerance of the species and
is affected by changes in shade tolerance with size (Kunstler et al., 2009).
RELIANCE ON CATASTROPHIC DISTURBANCE
IN NUTRIENT-RICH HABITATS
Three species of podocarps dominate the alluvial
floodplain forests of New Zealand, apparently contradicting the theory that podocarps are competitively excluded
from nutrient-rich sites. Dacrycarpus dacrydioides is a
dominant tree on poorly drained soils (Smale, 1984; Duncan, 1993; Norton, 1995), and Prumnopitys taxifolia and
Podocarpus totara are dominant on better-drained soils
(Esler, 1978; McSweeney, 1982). Establishment opportunities can be limited by near-continuous fern cover at some
sites (Coomes et al., 2005), and although smaller-seeded
angiosperms are able to take advantage of elevated sites
such as fallen trunks and tree fern stems, the larger-seeded
podocarps seldom establish in such niches (Lusk, 1995;
Christie and Armesto, 2003; Lusk and Kelly, 2003; Gaxiola et al., 2008). Indeed, none of these podocarps can regenerate continuously beneath mature rainforest canopies
(e.g., Urlich et al., 2005). Neither is gap-phase regeneration possible because tree fall gaps are colonized rapidly
by fast-growing woody angiosperms, ferns, and herbaceous plants, leaving few opportunities for slow-growing
trees (Coomes et al., 2005, 2009). Instead, slow-growing
podocarps are able to persist in the floodplain forests in
western South Island rainforests by regenerating after catastrophic disturbances, such as those resulting from debris
triggered by major movements of faults in the Southern
Alps and associated floods (Wells et al., 2001; Cullen et
al., 2003). The long life span of these podocarps allows
them to persist from one rare catastrophic disturbance to
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the next (Enright and Ogden, 1995; Veblen et al., 1995;
Lusk and Smith, 1998). Currently, regeneration failure
and ageing populations are observed over most of their
range (Holloway, 1954; Wardle, 1963b), and in some regions this could be because the last major movement of the
Alpine fault was nearly 300 years ago (ad 1717; Wells et
al., 1999). An event every few hundred years is sufficient
to maintain conifers as dominant elements (i.e., a “storage
effect” sensu Chesson, 2000). However, catastrophic regeneration of podocarps may be uncommon outside New
Zealand. Other species, such as the two Japanese species
in typhoon-affected forests, may benefit from disturbance
events by being relatively resistant to damage (see Dalling
et al., this volume).
Floodplain podocarps grow well in bare mineral soil
(e.g., Wardle, 1974) and presumably benefit from reduced
competition with angiosperms on fresh alluvium. However, they are not pioneer species, as they arrive after an
initial wave of colonization by early successional plants
(e.g., Reif and Allen, 1988). Woody plants such as Aristotelia serrata and Melicytus ramiflorus grow quickly and
form an open canopy; birds feed on the pseudo-arils of
podocarps and disperse the seeds into these early successional communities (Beveridge, 1964; Wardle, 1991). The
podocarps grow up beneath the open-crowned bushes
and trees and eventually overtop them (Beveridge, 1973),
continuing to colonize sites for many decades after disturbance (e.g., Wells et al., 2001). Interestingly, Dacrycarpus
dacrydioides and Prumnopitys taxifolia undergo a major
switch in leaf morphology at this stage, from having relatively broad leaves held in planes to having small leaves
on pendant branches (Atkinson and Greenwood, 1989).
These changes may be responses to increased light and
exposure once the trees have overtopped the early successional community (McGlone and Webb, 1981). New
Zealand has a disproportionate number of long-lived
podocarps that rely on flooding, although they are also
represented in Tasmania and mainland Australia (Barker,
1991; Gibson and Brown, 1991).
INTOLERANCE OF FIRE
Fire disturbance is usually fatal for podocarps, although two Australian podocarps (Podocarpus drouynianus and P. spinulosus) resist fire by sprouting from
belowground reserves (Chalwell and Ladd, 2005; Ladd
and Enright, this volume) and Halocarpus bidwillii can
regenerate after fire in New Zealand heathlands (Wardle,
1991). The increased frequency of fire since the arrival of
humans is thought to be the major factor of range contraction of podocarps in Australia (Hill and Brodribb, 1999),
and it all but annihilated forests formerly dominated by
podocarps in eastern New Zealand (McGlone, 2001).
Podocarps lack traits found in fire-adapted coniferous
lineages, such as serotinous cones, an ability to resprout
from the roots, and highly flammable leaves and litter. Several Podocarpus species have thin bark, suggesting that
their vascular cambium could be susceptible to damage
during fire. Highly flammable myrtaceous shrubs are the
early colonizers of burnt areas in the North Island of New
Zealand; the shrublands are soon colonized by podocarps,
but fire must be excluded for several decades in order for
the trees to overtop the shrubland and form a dense forest
(McKelvey, 1963; Ogden and Stewart, 1995; Wilmshurst
and McGlone, 1996).
RESPROUTING
Tall podocarp species do not, in general, resprout following damage (Martin and Ogden, 2006). For example,
in New Zealand forests there was no resprouting of Dacrydium cupressinum after logging, and regeneration was
dominated by resprouts of the angiosperm tree Weinmannia racemosa, to the disadvantage of D. cupressinum (Baxter and Norton, 1989). Saplings of D. cupressinum were
unable to recover after experimental clipping to simulate
deer browse because they resprouted poorly (Bee et al.,
2007). Typhoon-damaged trees of the podocarp Nageia
nagi in southern Japan were also ineffective at resprouting, in contrast to many co-occurring angiosperm trees
(Bellingham et al., 1996). Resprouting is more apparent
for temperate podocarps from poor sites, which are often
shrubs or small trees and exhibit multistemmed architecture. These include Halocarpus bidwillii, Lepidothamnus
intermedius, and Lagarostrobos franklinii, all of which
spread vegetatively in open habitats. By doing so, patches
of L. franklinii may have persisted for 10,000 years, and
trees within remnant populations are genetically homogenous (Clark and Carbone, 2008). Another tree of open
habitats, Phyllocladus alpinus, resprouts after wind damage (Martin and Ogden, 2006). A taller podocarp in
Chilean rainforests, Saxegothaea conspicua, exhibits vegetative regeneration, which is crucial for its maintenance
under shade-tolerant angiosperms in undisturbed stands
(Veblen et al., 1980; Lusk, 1996).
SUMMARY
Podocarps are ill equipped to compete with angiosperms in the race for light in canopy gaps. Some species
have evolved to tolerate prolonged shade, and these may
regenerate continuously under relatively open-canopied
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forest on poorer soils. However, few species can regenerate continuously under forests that are rich in shadetolerant trees, tree ferns, bamboos, or ground plants
because establishment sites are limited in these forests and
onward growth is severely hampered. In New Zealand,
three podocarp species dominate forests on rich alluvial
soils—they do this by escaping competitors when fresh
mineral surfaces are created by catastrophic disturbance
events. These events may occur every few hundred years,
and the long life spans of conifers allow them to persist
from one event to the next.
ECOLOGY OF TROPICAL PODOCARPS
The biogeography of tropical podocarps is dealt with
in other chapters but can be summarized as follows: podocarps are dominant elements of forests on a variety of soils
in the mountains of Papua New Guinea, Southeast Asia,
and subtropical and tropical Africa but are not dominant
in the mountains of northern Australia, New Caledonia,
and Madagascar and are only locally dominant in South
America. There are a few lowland species in Australasia,
the Pacific Islands, India, Africa, and the Americas; these
can dominate poor soils but are rare in other lowland forest types (P. J. Grubb, University of Cambridge, personal
communication; Wade and McVean, 1969; Enright, 1995).
TOLERANCE OF COLD AND HEAT
Tropical podocarps differ from those in temperate regions in being a major alpine element of tree lines
over a wide area (e.g., New Guinea; Grubb and Stevens,
1985), indicating that they are among the least warmthdemanding trees in the tropics. They are also among the
most tolerant, forming dense, almost pure stands immediately around frost hollow grassland (Grubb and Stevens,
1985). Like most temperate podocarps, they are excluded
from dry regions: although Afrocarpus falcatus is common in relatively dry forests of Africa, the overwhelming majority of species are restricted to the wet tropics.
Podocarps have easily distinguishable pollen, and the
observation that tropical podocarps prevail mostly in climates that are cool and wet is frequently used by palynologists to reconstruct paleoclimates. Thus, the spread
of podocarps into lowland Amazonia during Pleistocene
glaciations suggests cooler conditions in the basin (Colinvaux et al., 1996), whereas the upward migration of
podocarps into the páramo grasslands suggests a period of
warmer climate in the Peruvian Andes between 8900 and
3300 bp. As a further example, the waxing and waning
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of podocarp-rich rainforests across southeastern Australia during the late Pliocene and Pleistocene (Brodribb and
Hill, 2003b; Sniderman et al., 2007) and the Late Cretaceous (Gallagher et al., 2008) is interpreted in terms of
shifts in rainfall patterns driven by Milankovitch cycles
(greater summer insolation resulting in warmer tropical
seas, bringing greater rainfall to the continent).
SUCCESS ON POOR SOILS
Many tropical podocarps are restricted to poor soils.
In the appendix we provide brief descriptions of 96 species
of tropical, subtropical, and warm temperate podocarps,
taken mostly from Earle (1997–2009). We categorized each
species as either (1) restricted to outstandingly poor soils,
(2) restricted to rich soils, or (3) found on both rich and
poor soils. “Outstandingly poor soils” included ultramafic
soils, podzolized sands, peats, and shallow soils associated
with limestone, sandstone, coastal bluffs, and ridgetops. We
also included species associated with tree lines in the outstandingly poor soils category, the soils being highly organic
and probably with markedly low rates of nitrogen mineralization (P. J. Grubb, pers. comm.). We subdivided their
habitats into montane and lowland rainforest species (montane is defined here as >1,000 m elevation in the tropics and
>800 m in the subtropics and warm temperate regions).
Most tropical podocarps in Earle’s database are found
in mountains (56%), so the majority of the species occupy
cool climates. Several of these species (21) are described
as locally common, dominant, or forming pure stands at
high altitude, on ridges and sometimes in peats. They include Dacrycarpus (3), Dacrydium (7), and Podocarpus
(9). Half of the montane species are also found in “normal” montane forests as well as on poor soils, but they are
often less common when off the poorest soils: this group
includes all seven species of Dacrycarpus. Nine species appear to be restricted to “normal” montane forests (i.e.,
they are not mentioned as growing on poor soils in their
ecological descriptions).
In the lowlands, 11 species are restricted to extremely
poor soils, 12 are common on poor soils but venture into
forest on better soils, and 9 are found in “typical” lowland
rainforest. The last group comprises three genera: Nageia
(3), Podocarpus (5), and Parasitaxus (1). The Nageia species
are shade-tolerant trees of warm temperate and subtropical
forests (Kohyama, 1986) and are canopy species that are
“scattered” and “often common” in the forest understory.
The Podocarpus species are described as “scattered” and
“locally common,” and all are subcanopy (~25 m tall), except P. spinulosus, which is a shrub restricted to sheltered
coastal sites and gullies. Finally, Parasitaxus usta (New
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Caledonia) is the only parasitic gymnosperm and never
grows taller than 2 m; it persists in shade by virtue of the
carbon it gains by parasitism on the roots of Falcatifolium
taxoides. The 11 species restricted to poor soils are found
on peat swamps, kerangas, and ultramafics; they include
Dacrydium (3), Falcatifolium (2), and Podocarpus (6). Six
of these species are small trees (<12 m tall).
Presumably, podocarps are successful on the poorest
tropical soils for the same reasons as in temperate regions.
The species restricted to the poorest soils are significantly
shorter and have much smaller leaves than species of better soils (e.g., Aiba and Kitayama, 1999), with species associated with both soil types having intermediate height
and leaf area (Table 7.1; significance based on analysis of
variance). These patterns are observed in both lowland
and montane forests. The trend is precisely as anticipated,
given that asymmetric competition for light is less intense
among plants growing on poor soils, so height growth is
not as strongly advantageous, and small leaves held on
upright stems are effective for whole-plant photosynthesis
within open forest. In lowland and lower montane forests, the heights achieved by podocarps are unremarkable,
but at high altitude the species are often emergent. The
area of shade leaves (as a ratio of the area of sun leaves)
was 2.4 ± 0.10 (r 2 = 0.85), with no evidence of variation
among forest or soil types (Table 7.1). A shift from big,
shade-tolerant juvenile foliage to smaller adult foliage is
observed in many tropical podocarps, especially canopy
emergents, just as seen in temperate species.
as a group (Morley, this volume). Nitrogen and phosphorus are likely to be increasingly limiting in the mountains
(Grubb, 1977), to the benefit of podocarps. Podocarps may
be particularly effective at photosynthesis in the persistently
cloudy conditions often encountered on tropical mountains. Using a physiological modeling approach, Whitehead
et al. (2004) found that carbon uptake by Dacrydium cupressinum in lowland New Zealand is greater than that of
oak trees in the United States when conditions are overcast
and the diffuse fraction of incoming radiation is high.
There is little published information on regeneration
processes and size structure of tropical montane podocarp populations (but see other chapters in this volume).
Podocarpus urbanii in Jamaican montane rainforests is
most common on less-fertile soils, although not on highly
acidic mor soils (Tanner, 1977). It exhibits continuous regeneration in these forests but does not have a reverse-J
distribution (Bellingham et al., 1995). Jamaican forests are
frequently affected by hurricanes, but P. urbanii, like the
two podocarp species in typhoon-affected Japanese forests, is resistant to hurricane disturbance (Bellingham et
al., 1995). Following hurricanes, the growth rate of P. urbanii is faster than that of angiosperm trees, possibly because it survives storms relatively unscathed (Dalling et
al., this volume; E. V. J. Tanner, University of Cambridge,
personal communication). In addition, abundant seedlings
and saplings of podocarps are found in the understory of
high-altitude forests in New Guinea (Wade and McVean,
1969), suggesting that the species are sufficiently shade
tolerant to regenerate under the canopy. Aiba et al. (2004)
compared 42 common species, including four podocarps,
in a plot at 1,560 m altitude in Kinabalu Park, Borneo.
Two podocarp species were most common on ridges
(Phyllocladus hypophyllus and Dacrydium pectinatum),
whereas the other two were less restricted by topography
SUCCESS IN MOUNTAIN ENVIRONMENTS
It is not surprising that podocarps are prominent in
tropical montane forests: these are the environments most
similar to temperate environments in which they evolved
TABLE 7.1. Relationship of mean height and mean leaf area of canopy of leaves to forest and soil type. All data were extracted from
descriptions provided by Earle (1997–2009); N is the number of species contributing to each mean. Leaf areas were estimated from
mean widths and lengths assuming an elliptical shape, and the largest height was used whenever a range was given.
Forest type
Tropical lowland
Tropical montane and warm temperate
Cool temperate
Soil
N
Height
(m)
Leaf area
(cm2)
Understory to canopy
tree leaf area ratio
Poor soils
Mostly poor
Better soils
Poor soils
Mostly poor
Better soils
All soils
9
11
8
17
14
9
25
14.9 ± 2.8
25.5 ± 5.1
27.5 ± 4.8
19.2 ± 2.7
24.6 ± 3.8
26.2 ± 3.6
14.9 ± 2.8
4.7 ± 1.7
5.1 ± 3.5
9.0 ± 3.4
1.9 ± 0.8
4.7 ± 1.6
4.1 ± 1.5
1.1 ± 0.5
3.2 ± 0.8
3.1 ± 0.8
3.3 ± 1.3
4.1 ± 0.6
2.3 ± 0.3
3.1 ± 1.0
4.3 ± 0.9
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(Dacrycarpus imbricatus and Falcatifolium falciforme).
All podocarp species except Falcatifolium falciforme had
a greater proportion of their crowns in exposed positions
within the canopy than predicted by chance, suggesting
that they were light demanding. In contrast, Falcatifolium
falciforme had a greater proportion of its crowns in shaded
positions and a population structure indicating that the
species was shade tolerant (Kitayama et al., this volume).
RARITY IN LOWLAND TROPICAL
SITES ON BETTER SOILS
Podocarps are absent from much of the lowland tropics,
except on poor soils, although they are rare components
of Australasian tropical lowland and lower montane forests (Enright, 1995). Two widespread species, Podocarpus
neriifolius and Nageia wallichiana, reach densities of only
1–2 per hectare within the 700–1,500 m elevation band of
New Guinean mountains and are usually observed as solitary trees with few seedlings nearby (Enright, 1995). We
reason that three factors conspire to exclude podocarps:
(1) The high leaf area index of the lowland tropical forests
means that the understory is too deeply shaded to allow
even the most shade tolerant of podocarps to regenerate,
the exception being Nageia species, which have large, multiveined leaves (mean for lowland species = 48 cm2) similar to those of Gnetum (another gymnosperm of rainforest
understories). (2) Podocarps are outcompeted in the race
for light in tree fall gaps. Tropical podocarps may well
grow faster than temperate relatives—their wood contains
wider tracheids (Lusk, this volume) and is significantly less
dense (Figure 7.1)—but it is inconceivable that they could
compete with the growth of light-demanding angiosperms,
which can reach upward of 1 m a year (e.g., Richards and
Williamson, 1975). For example, a gap-demanding angiosperm, Toona australis, was found to have greater stomatal
conductance and leaf-specific stem hydraulic conductivity
than two tropical podocarps (Nageia fleuryi and Podocarpus grayii) and grew much more rapidly than the podocarps in full sun (1,300–1,800 µmol m-2 s-1) (Brodribb
et al., 2005). Finally, (3) opportunities for catastrophic regeneration are taken by angiosperms. Among the lowland
tropical podocarps, two New Caledonian trees, Dacrycarpus vieillardii and Podocarpus polyspermus, appear to be
exceptions and are maintained by disturbance, colonizing
floodplains in a way similar to D. dacrydioides and P. totara in New Zealand (Jaffré, 1995). For most of the lowland tropics this niche is taken by angiosperm trees, some
of which are long-lived (e.g., Ceiba pentandra). Other regeneration niches associated with disturbance seem to be
taken by angiosperms. For example, the “shade-persistent
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pioneer” strategy of the long-lived angiosperm tree Alseis
blackiana in lowland rainforests in Panama (Dalling et al.,
2001) is analogous to some long-lived podocarps (e.g.,
Podocarpus totara) in New Zealand rainforests.
Most tropical podocarp species are intolerant of fire,
like their temperate cousins. In the Dominican Republic,
fire virtually excludes Podocarpus aristulatus from forests
above 1,800 m, which are dominated by Pinus occidentalis.
Fires are prevalent during El Niño droughts in these forests
(every seven years or so), and they also have lower temperatures and precipitation than the cloud forests at lower
altitude (1,550–1,800 m), which do not support fire and
in which P. aristulatus is the third commonest tree (Martin and Fahey, 2006; Martin et al., 2007). Similarly, the
páramo grasslands of the Andes have spread in response
to frequent burning during the last 8,000 years, and podocarps are now restricted to montane forests well away from
the grasslands (Niemann and Behling, 2008). Increased
fire frequency since the arrival of humans is thought to be
the major driver of podocarp extinction in Australia (e.g.,
Dacrydium from tropical north Queensland; Lynch et al.,
2007). A few tropical podocarp species are capable of persisting in habitats that burn. Dacrycarpus compactus, Dacrycarpus expansus, and Dacrydium novo-guineense are all
locally prominent components of tree fern grasslands and
thickets that occur near tree lines on tropical mountains,
even though indigenous peoples burn these areas. Corlett
(1984) noted that Dacrycarpus compactus has thick bark,
which might afford it some protection.
CONCLUDING THOUGHTS
Tropical and temperate podocarps function much as
Bond envisaged: they are slow-growing tortoises. Most
tropical species are restricted to montane forests with low
total leaf area or lowland sites with exceptionally poor
soils. Competition for light is less intense in such forests,
and podocarps compete effectively by efficient capture
and retention of nutrients. In addition, genera with small
leaves held on erect/pendent stems may also achieve high
rates of whole-plant photosynthesis in open canopied forests that prevail on poor soils. On richer soils in the tropics, slow-growing podocarps are incapable of competing
with angiosperms in the battle for light in tree fall gaps.
Some species may be capable of tolerating deep shade and
surviving for many years in forest understories, but regeneration is not possible unless there is significant height
growth, and that is severely hampered by shading. The
simplest hypothesis is that the leaf area indices of lowland
tropical forests are simply too high to allow regeneration
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of imbricate-leaved podocarps, whereas broad-leaved species with anastomosing veins (Nageia and some Podocarpus) are so shade tolerant that they regenerate beneath
closed canopies. Measurement of growth and survival of
podocarps in contrasting tropical forest types, in conjunction with demographic models (e.g., Kunstler et al., 2009),
would help resolve this issue.
ACKNOWLEDGMENTS
We are grateful to Macarena Cardenas, Neal Enright, Martin Gardner, Will Gosling, Peter Grubb, Chris
Lusk, and Ed Tanner for sharing some of their thoughts
on tropical podocarp ecology and to Will Simonson for
proofreading the manuscript. We thank Chris Earle for
compiling the Gymnosperm Database, quoted extensively
in the appendix, and for providing many suggestions on
the manuscript. PJB was funded by the New Zealand
Foundation for Research, Science, and Technology (Ecosystem resilience OBI).
APPENDIX:
DESCRIPTIVE ACCOUNTS OF
PODOCARPS FROM TROPICAL,
SUBTROPICAL, AND WARM
TEMPERATE REGIONS
Descriptions are taken primarily from Earle (1997–
2009), who sourced his data from various primary references, and also from personal communications with P. J.
Grubb. Information on Andean and Amazonian species
in the last section was sourced from Jorgensen and LeonYanez (1999). Tree heights (H) are given after each description; where a range of heights for different habitats is
published, the largest is quoted.
LOWLAND TROPICAL RAINFORESTS
Common on Poor Soils but Not Restricted to Them
Dacrycarpus vieillardii. New Caledonia. Grows
throughout the main island on serpentine soils along riverbanks, in moist depressions, and in frequently flooded
areas from sea level to 900 m above sea level. Similar in
ecology to D. dacrydioides of New Zealand. H = 25 m.
Dacrydium balansae. New Caledonia. Occurs in the
drier parts of forests, normally on serpentine soils from
sea level to 1,000 m. A few specimens from ombrophilous
forest were 20 m tall trees. H = 12 m.
Dacrydium guillauminii. New Caledonia. Found
within a few kilometers along two rivers. H = 2 m.
Dacrydium magnum. Solomon Islands, Moluccas.
Locally common in the canopy of moist tropical forest between 60 and 1,200 m. Often along ridge crests, where it
has a somewhat reduced stature. H = 30 m.
Dacrydium nidulum. Fiji, New Guinea, Moluccas, Celebes, Lesser Sunda Islands. Common in the western parts
of New Guinea, but elsewhere populations are mostly
rather isolated. A canopy tree of primary and sometimes
secondary rainforest from sea level to 1,200 m, but mostly
under 600 m. In Fiji it forms open, low-growing, monodominant stands of stunted trees and is also a component
of mesic forests (Keppel et al., 2006). H = 30 m.
Dacrydium pectinatum. Hainan, China, Malesia, Borneo, Philippines. Scattered large individuals are found in
primary rainforest other than dipterocarp forest from sea
level to 1,500 m, but mostly below 600 m. Dense stands
are found in boggy areas, and nearly pure stands of stunted
trees occur in shallow sandy soils, especially on degraded
heath forests (“padangs”) and on kerangas in heath forest.
In Sabah it grows on ultramafic soils; in Brunei it grows in
pure stands in the center of peat swamps. H = 40 m.
Nageia maxima. Borneo (Sarawak). Locally common
in the understory of rainforest on ridges in Bako National
Park and in the peat swamp forest, from ~0 to 120 m.
H = 10 m.
Nageia motleyi. Southern Thailand, Malesia (Malaya, Sumatra, Borneo). Scattered in primary and secondary rainforest, from very low altitude (15 m) to ~500 m.
Occurs not only on slopes and hills on dry soil but also
in Borneo in other situations: in Sarawak on deep peat
in a mixed ramin-peat swamp, on ridges and hillsides in
bindang-dipterocarp forest, and at 1,000 m on podsolic
sandy loam. H = 54 m.
Podocarpus confertus. Malesia. Subdominant in
somewhat open and sometimes stunted forest. Found in
dense local populations on various poor soils, some or
most of which are ultrabasic. H = 36 m.
Podocarpus insularis. New Hebrides, Solomon Islands, New Britain, New Guinea and adjacent islands.
Scattered and locally common in wet rainforest, also in
Nothofagus forest with undergrowth of Nastus from near
sea level to 1,680 m, and as smaller trees in low ridge habitats. H = 39 m.
Podocarpus neriifolius. Nepal, Sikkim, India, Thailand, Vietnam, Malaysia, Indonesia, Philippines, Celebes,
Lesser Sunda Islands, Moluccas, New Guinea, New Britain, Solomon and Fiji islands. Scattered and locally common in primary rainforests from near sea level to ~2,100
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m. In most areas it appears as an understory tree with occasionally much larger, emergent specimens in the canopy,
but in other areas it is normally a canopy tree. Various
habitats (often on rocky hilltops, in mossy forest, and
swampy forests but rarely riverine) and on various soils
(limestone, kerangas in heath forest, sandstone ridges, and
laterites, sandy clay, ultrabasic). H = 30 m.
Retrophyllum minus. New Caledonia. Southern part
of island on ultramafic soils, at elevations of up to 200
m above sea level. A water-dependent plant (rheophyte)
inhabiting riparian habitats, in this case lakes and riverbanks in shallow water. H = 3 m.
Restricted to Poor Soils or Open Forest
Dacrydium araucarioides. New Caledonia. Locally,
a dominant species in the vegetation on serpentine soils,
from sea level to 1,150 m. H = 6 m.
Dacrydium elatum. Vietnam, Laos, Cambodia, Thailand, Malaya, Sumatra, Borneo. Scattered in moist rainforest, from sea level but mostly above several hundred
meters to 1,700 m. Grows most abundantly in open situations, indicating a preference for disturbed conditions. It
also appears to prosper on difficult soils (sandstone, granite, kerangas). Does not enter into high mountain scrub.
H = 40 m.
Dacrydium nausoriense. Fiji. In slightly open forest
on the leeward sides of the large islands of Fiji and apparently of limited extent. H = ?
Falcatifolium angustum. Borneo. Found at 90–240 m
on podsolized sands and kerangas. H = 20 m.
Falcatifolium falciforme. Malaya, Borneo. Locally
common along ridges as a bushy tree or in the subcanopy
of primary rainforest, often on podsolic sands and kerangas, but occasionally on deeper fertile soils. Somewhat
emergent forest giant, from 400–2,100 m. H = 12 m?
Podocarpus beecherae. Southern New Caledonia.
Maquis vegetation on ultrabasic soil (generally toxic to
plants and the reason for the stunted plants of the maquis)
at low elevation. H = 6 m.
Podocarpus costalis. Philippines and other islands between Luzon and Taiwan. On coastal bluffs from sea level
to at least 300 m elevation. H = 5 m.
Podocarpus globulus. Borneo. Found in primary rainforest or moss forest on ridges and peak at 300–1,500 m
elevation in areas where the forest is not dominated by
dipterocarps. Adapted to ultramafic soils. H = 27 m.
Podocarpus micropedunculatus. Borneo. From 0 to
500 m elevation scattered in Agathis forest understory
or in thickets at the edges of clearings. Mostly on sandy,
•
133
podzolic soils, kerangas, sandstone, humic peaty podzols
of raised beaches, and peat swamp forests. H = 7 m.
Podocarpus polystachyus. Thailand, Malaysia (Malay Peninsula), Borneo, Philippines, Moluccas, west New
Guinea. Mainly at low altitudes in three distinct habitats: (1) sandy beaches, often gregariously bordering the
sea at high-tide mark, sandy coastal bluffs and low outcrops, and also sandy ridges in mangroves; (2) on lowland
coastal kerangas and sandy pandangs (degraded heath
forest) and sandy heath forest; and (3) on limestone hills
inland. H = 20 m.
Podocarpus teysmannii. Malaysia, Indonesia. An understory tree in primary or secondary rainforest at elevations up to 1,140 m. In Banka it grows on granite sands.
H = 12 m.
Apparently Associated with Rainforests
on Relatively Fertile/Deep Soils
(No Mention of Poor Soil in Description)
Nageia fleuryi. China (Guangdong, Guangxi, and
Yunnan), Cambodia, Laos, Vietnam (mountainous provinces). Occurs sparsely in primary and slightly disturbed
evergreen rainforests at elevations of 200–1,000 m. At
Cuc Phuong and Cat Ba National Parks, the species occurs
in groups and is the main species in some stands. A lightdemanding species thriving well on good sites with deep,
well-drained soils developed from limestone. H = 25 m.
Nageia nagi. Japan, China, Vietnam. Grows in tropical evergreen broad-leaved forest, on hills or mountains
below 1,000 m elevation. Neutral, shade-demanding tree
when young. When mature, may become a canopy dominant. Associated with ferralitic, deep and fertile, loamysandy soils. H = 30 m.
Nageia wallichiana. India (Assam), Burma, Thailand,
Indochina, China (Yunnan), Malesia (Sumatra, Malaya,
Banka Island, western Java, Lesser Sunda Islands, Borneo, Philippines, north and central Celebes, Moluccas),
New Guinea. Scattered and often common (but nowhere
reported as gregarious or dominant) in primary rainforests from very low elevation (5 m), ascending occasionally as high as 2,100 m. Widely distributed in southern
China, growing on neutral or slightly acidic soils, tolerating shade. One of the tallest trees in the forest, but perhaps
barely emergent. H = 54 m.
Parasitaxus usta. New Caledonia. Found at 400–
1,100 m elevation. This is the only known parasitic gymnosperm. H = 1.8 m.
Podocarpus ledermannii. New Guinea, New Britain. Scattered and locally common in the understory of
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primary rainforest from low elevation to at least 1,800 m.
H = 26 m.
Podocarpus levis. Eastern Borneo, Celebes, Moluccas,
New Guinea. Scattered and locally common in primary
rainforest, from sea level to 1,650 m. In eastern Borneo on
limestone. H = 25 m.
Podocarpus nakaii. Taiwan. Scattered as a subcanopy
tree in broad-leaved forests in the northern and central
parts of the island. H = ?
Podocarpus spathoides. Solomon Islands, eastern
New Guinea, northern Moluccas, Malaya. Scattered and
locally common at 1,000–1,200 m in the two western
stands and near sea level in the east. Recent field work indicates that “P. spathoides” in the Solomon Islands (which
occurs at sea level) is sufficiently distinct to be described as
a new species (M. Gardner, Royal Botanic Garden Edinburgh, personal communication). H = 30 m.
Podocarpus spinulosus. Australia (New South Wales
and Queensland). A shrub in sheltered coastal sites and
gullies on the adjacent ranges. H = 3 m.
MONTANE TROPICAL RAINFORESTS
Common on Poor Soils but Not Restricted to Them
Dacrycarpus cinctus. Central Celebes, Moluccas,
New Guinea. In New Guinea extremely common and often dominant or codominant with Nothofagus, Libocedrus, Elaeocarpus, and Podocarpus, in mountain forest
and mossy forest. On Mount Binaja in orchard-like pure
stands with a mossy ground cover. Rarely in muddy parts
of swamps. A canopy tree or sometimes emergent, often
thick trunked at 1,800–2,850 m. Occasionally reaches
3,600 m; in Ceram occurs at 1,300–3,000 m. H = 33 m.
Dacrycarpus compactus. New Guinea. In subalpine
shrubberies and alpine grasslands, 3,200–3,800 m. Common on the higher peaks near the tree line, sometimes
forming pure stands, emerging above a subalpine shrubbery, or scattered in alpine grassland often as isolated
specimens and obviously fire resistant. A component of
Podocarpus–Libocedrus forest, rarely on wet peaty soil,
at 2,800–3,950 m, but mostly above 3,400 m. H = 20 m.
Dacrydium beccarii. Solomon Islands, New Guinea,
Moluccas, Philippines, Borneo, Malaya, northern Sumatra. In the eastern part of the range there are only widely
separated occurrences, and even in the western part they
are somewhat discontinuous. Most common as a shrub or
small tree on mossy ridges where it is often dominant, but
also found rising above a low, mixed mountain scrub at
600–2,500 m. A variety of soils have been indicated. H = ?
Dacrydium gibbsiae. Borneo. Common on the slopes,
being codominant on ultrabasic soils in the mountain
mossy forest at 1,500–3,600 m. H = 12 m.
Dacrydium gracile. Borneo, Sarawak. Rows scattered
in the canopy of mountain rainforest. In Sarawak also in
heath forest on sandstone. Rare. H = 30 m.
Dacrydium xanthandrum. Solomon Islands, New
Guinea, Celebes, Philippines, Borneo, northern Sumatra.
Locally discontinuous. Locally common or even dominant
and shrubby on mossy ridges with peaty soils over clay,
sand, granite, sandstone, or dacite. Also scattered as trees
in nearby primary forest from (500–)1,000–2,700 m. H = ?
Falcatifolium taxoides. New Caledonia. An understory tree in the wet forests on ultramafic soils of the main
island. H = 15 m.
Phyllocladus hypophyllus. Philippines, Borneo, Celebes, Moluccas, New Guinea. Moist mountain forests
sometimes as low as 900 m up to the tree line at 3,200–
4,000 m. Scattered in the forest at lower elevation where
trees may be quite large. More common but of reduced
stature at higher elevations. In New Guinea it is a widespread and common species from the upper lowland forests to the subalpine shrubberies, rarely as a solitary tree in
the alpine grasslands (900–3,600 m). H = 30 m.
Podocarpus laubenfelsii. Borneo, Sabah, eastern Kalimantan. Scattered in primary rainforest and moss forest,
growing as a large emergent on rocky ridges on kerangas.
Dominant in heath forests and on waterlogged acid soils
of Agathis forests. H = 35 m.
Podocarpus pseudobracteatus. New Guinea. Scattered and locally common in the understory of mossy
Castanopsis-Nothofagus forest and Dacrydium swamp
forest, sometimes entering the alpine shrubbery. H = 15 m.
Podocarpus rotundus. Eastern Borneo, Philippines.
Found in dwarf mossy forest, at about 1,000–2,200 m.
H = 15 m.
Podocarpus rubens. Sumatra, Celebes, Lesser Sunda
Islands, New Guinea. Scattered as a medium-sized tree in
primary rainforest, mostly above 1,500 m but as low as
800 m on smaller islands. Otherwise locally common to
dominant as a small tree on ridges at 2,000–3,000 m or
occasionally higher. Mostly on latosols. In New Guinea in
fagaceous mossy forest, rarely in swampy forest on peaty
soils with Dacrydium. H = 30 m.
Podocarpus smithii. Australia (Queensland). Endemic
and highly local in montane rainforests on the eastern
Atherton Tableland. Usually grows along creeks at mid
elevations (900–1,200 m), often on granitic soils. H = 30.
Podocarpus urbanii. Jamaica. Montane rainforests
of the Blue Mountains (1,370–2,250 m) across most soil
number 95
types, but most abundant on those of low, but not lowest,
available nitrogen and phosphorus. H = 15 m.
Sundacarpus amarus. Australia (northeastern coastal
Queensland), New Guinea, Moluccas, Lesser Sunda Islands, Java, central and southwestern Celebes, Philippines,
Borneo, Sumatra. In Queensland primarily in the Atherton Tableland on basaltic soils at 600–1,200 m. Scattered
and often common in primary and secondary rainforest.
Very common in New Guinea, often in fagaceous forest,
sometimes in mossy forest or submontane forest at ~900
m (with Dysoxylum, Macaranga, and Ficus), where it can
be emergent as a colossal tree. Often on latosols, rarely on
sandy soils or on marshy ground. Occurs from sea level
but mainly at 500–2,000(–2,300) m. H = 60 m.
Restricted to Poor Soils or Open Forest
Dacrydium comosum. Malaya. On exposed ridges as
a local dominant in stunted mossy forest at 1,440–2,200
m. H = 4 m.
Dacrydium ericoides. Malesia. Locally common in
primary forest on exposed mossy ridges at 1,000–1,500
m. H = 17 m.
Dacrydium lycopodioides. New Caledonia. At elevations of 900–1,400 m in ombrophilous forests on the
southern part of the main island. H = 25 m.
Dacrydium medium. Malaya, northern Sumatra. Shrub
or small tree rising above and often dominant in low mountain scrub on what appears to be rather poor soils at 960–
2,100 m in Malaya and 1,800–2,600 m in Sumatra. H = ?
Dacrydium novo-guineense. Celebes, Moluccas, New
Guinea. Long, mossy crests and in open areas at 700–3,000 m,
but mostly 1,500–2,200 m. Rising above the mid-mountain
canopy or a common small tree at higher elevations rising
above ferns and other scrub often after fire. Sometimes dominant. On different soil types: clay, stony sand. H = 29 m.
Falcatifolium gruezoi. Philippines, Celebes, Moluccas.
In exposed locations along ridges or on the borders of open
areas. At 1,600–2,200 m in the Philippines, 1,200–1,400
m in Celebes, and 700 m in Obi (Moluccas). H = 12 m.
Podocarpus archboldii. New Guinea. Mainly found
in upper lowland regions to upper montane areas and occasionally in the subalpine shrubberies (800–3,100 m).
H = 40 m.
Podocarpus brassii. New Guinea. Usually found in upper montane and subalpine regions, sometimes venturing
out into the alpine grasslands. Also as a survivor of burned
subalpine shrubberies replaced by grassland. H = 15 m.
Podocarpus crassigemmis. New Guinea. Common or
subdominant in the canopy of high-mountain mossy forest
•
135
or emergent. Often in Nothofagus and Phyllocladus forest, rarely in secondary forest, and occasionally in grassland. H = 38 m.
Podocarpus deflexus. Malaysia (northern Sumatra,
Malaya). Rising above and locally dominant in dwarf
mountain scrub at 1,500–2,100 m. H = 10 m.
Podocarpus gibbsiae. Borneo. At 1,200–2,400 m elevation, typically on moss forest ridges. Mostly or always
on ultramafic soils. H = 20 m.
Podocarpus glaucus. Solomon Islands, New Guinea,
Moluccas, Philippines. A medium-sized tree in the forest
or more often dwarfed or even decumbent on mountain
crests in stunted mossy forests. Often locally common,
(500–)1,000–2,800 m. Recorded from stony, sandy clay
and from a limestone ridge associated with Gymnostoma
and Rhododendron on peaty soil. H = 15 m.
Podocarpus gnidioides. New Caledonia. Above 600
m elevation on rocky ridges in the mountains. H = 2 m.
Podocarpus ridleyi. Malaysia. Localized and more or
less dominant on several isolated peaks with poor soils in
a somewhat stunted rainforest, at 480–1,300 m. On ridges
over sandstone and on granite. H = 24 m.
Retrophyllum comptonii. New Caledonia. Ombrophilous forests on ultramafic soils throughout the main island at 750–1,450 m. H = 30 m.
Apparently Associated with Rainforests
on Relatively Fertile/Deep Soils
(No Mention of Poor Soil in Description)
Dacrycarpus imbricatus. Northern Burma, far southern China, Vietnam, Laos, Malaya, Philippines, Sumatra,
Borneo, Java, Celebes, Moluccas, Lesser Sunda Islands,
New Guinea, New Hebrides, Fiji. Mostly scattered and
common in primary and secondary rainforest. In West
Java codominant with Podocarpus neriifolius and Altingia noronhae, on the south slope of Mount Tjeremai
volcano characterizing the zone between 2,400–2,700
m, unexplainably without other codominants. In Timor
found under more or less seasonal conditions as isolated
specimens laden with Usnea in grassland after deforestation, mostly at 1,000–2,500 m. In Lombok reported at
as low as 200 m, and in Celebes ascending to 3,000 m.
Probably exterminated at lower elevations by deforestation. In China in mixed forests or pure stands on slightly
acidic yellow earth soils in valleys of montane streams at
400–1,500 m. H = 50 m.
Dacrydium spathoides. New Guinea. Growing as a
canopy tree at 2,150–2,200 m in moist, mossy mountain
rainforest. H = 34 m.
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Falcatifolium papuanum. New Guinea. Grows in the
understory of moist mountain forests at 1,500–2,400 m.
Typical associates include Nothofagus, Myrtaceae, and
other Podocarpaceae. H = 22 m.
Podocarpus dispermus. Australia (Atherton Tableland). In rainforest, not plentiful. H = 20 m.
Podocarpus macrocarpus. Philippines. Scattered and
sometimes common in cloud forests, ~2,000–2,100 m.
H = 20 m.
Podocarpus macrophyllus. Southern Japan, Burma,
China, Taiwan. Virgin broad-leaved forest dominated by
over 20 m tall trees of Lauraceae and Fagaceae. H = 15 m.
Podocarpus magnifolius. Eastern Venezuela to Bolivia. Widely distributed in cloud forest at 800–1,600 m.
H = 25 m.
Podocarpus neriifolius. Vietnam. Occurs as scattered
individuals in remaining primary forests in remote areas,
growing sparsely along water courses, usually mixed with
broad-leaved species, such as Fokienia hodginsii, Celtis
australis, Altingia siamensis, Cinnamomum spp., Gironniera subaequalis, Mallotus yunnanensis, Castanopsis,
and Lithocarpus spp. It chiefly appears on humid, fertile, especially sandy soils, but also on clayey-stony soils.
H = 25 m.
Podocarpus rumphii. Philippines, Taiwan. Scattered
in broad-leaved forests at medium altitudes. H = 30 m.
Prumnopitys ladei. Australia (Atherton Tableland,
Queensland). Rainforests on granite-derived soils at
1,000–1,200 m. H = 25 m.
Retrophyllum rospigliosii. Western Venezuela, Eastern Colombia, central Peru. Native to the wet forests of
the Andes, it grows best at 500–3,500 m, needing constant
humidity and cloudiness. Develops best on gentle slopes,
fertile river lowlands, plateaus, and small depressions.
Grows in wet, clay or clay-sand, deep, relatively fertile
soils with good to slow drainage and acidic pH. H = 30 m.
INSUFFICIENT INFORMATION AVAILABLE
Dacrycarpus cumingii. Widespread in Philippines,
northern Sumatra; rare in Borneo. Locally common at
elevations of (1,000–)1,850–2,650(3,314) m in primary
moss forest. H = 25 m.
Dacrycarpus expansus. Papua New Guinea (Central
Highlands). Locally common or even in pure stands or
codominant, sometimes emergent. Often in (human) disturbed situations, such as on edges of tree fern grassland,
1,300–2,750 m. H = 25 m.
Dacrycarpus kinabaluensis. Borneo. Common, growing in sometimes pure stands in dwarf mountain scrub at
elevations from about 2,700 m to the tree line at about
4,000 m. H = 13 m.
Dacrycarpus steupii. Central eastern Borneo, central
Celebes, New Guinea. Locally common, particularly in
disturbed forests, or in poorly drained areas where it may
form nearly pure stands. In boggy grasslands and reed
swamps, on sandy clay, once on a rocky riverbank, once
on a limestone hillock in mossy forest (Mount Beratus).
Elevations of 860–3,420 m, but mostly ~1,500–2,000 m.
H = 35 m.
Dacrydium cornwallianum. New Guinea. Dominant
to nearly pure stands in swamp forests and perhaps also
mossy heath forests at 1,450–2,300 m. H = 30 m.
Dacrydium leptophyllum. Western New Guinea.
Known only from the top of Mount Goliath at 3,000–
3,600 m. H = ?
Prumnopitys standleyi. Costa Rica. At 2,000–
3,200 m, in areas with 2,000–4,000 mm annual rainfall
and temperature range of 3°C–25°C. H = 25 m.
Podocarpus sellowii. Brazil. Extremely broad and
scattered range, occurring in montane vegetation. Typical
of montane areas in the tropical coastal range rainforest
(Mata Atlántica) and rarely occurs within Araucaria angustifolia forests. H = ?.
Podocarpus acuminatus. Brazil. H = 4.5.
Podocarpus atjehensis. Northwestern Sumatra, New
Guinea. H = 15 m.
Podocarpus borneensis. Borneo. Locally common
or even dominant on mossy rocky ridges or scattered in
nearby forest, in high kerangas forest and on white, sandy
soils. Elevations of 700–2,070 m; one collection from a
swamp at 360 m. H = 12 m.
Podocarpus bracteatus. Indonesia, Java, Lesser Sunda
Islands. H = 40 m.
Podocarpus brasiliensis. Brazil, Venezuela. Mountains
and in few hectares of wetland in the middle of the massive Cerrado. H = 15 m.
Podocarpus brevifolius. Philippines, Indonesia, China
(Guangxi and Guangdong), Vietnam. Usually growing on
limestone. H = 15 m.
Podocarpus buchholzii. Venezuela. H = 7 m.
Podocarpus glomeratus. Andes. Elevations of 2,500–
4,000 m. H = ?
Podocarpus ingensis. Andes. Elevations of 1,000–
3,000 m. H = ?
Podocarpus lambertii. Argentina, Brazil. H = ?
Podocarpus lophatus. Philippines. Mossy forest at
1,800 m elevation. H = ?
Podocarpus matudae. Mexico, Guatemala. Large
tree. H = ?
number 95
Podocarpus roraimae. Mountains bordering Venezuela and Guyana. Endemic. Elevations of 1,800–2,400 m.
H=?
Podocarpus sprucei. Andes. Elevations of 2,000–
4,000 m. H = ?
Podocarpus steyermarkii. Venezuela, Guyana. H = 25 m.
Podocarpus tepuiensis. Eastern Venezuela. Endemic
shrub or small tree. H = ?
Podocarpus woltzii. Madagascar. H = 20 m.
Prumnopitys montana. Andes. Elevations of 1,500–
4,000 m. H = ?
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