910
Tree seedling growth and survival over 6 years
across different microsites in a temperate rain
forest
P.J. Bellingham and S.J. Richardson
Abstract: We investigated whether canopy tree seedlings have different growth and mortality rates on different microsites
in montane rain forests of the western South Island, New Zealand. Seedling relative height growth rates of three species,
Podocarpus hallii, Quintinia acutifolia, and Weinmannia racemosa, were very low (mean = 0.037 cm·cm–1·year–1).
Seedling growth rates were higher on logs than on the ground at high light levels, but the probability of seedling death
on logs was also greater at high light levels. Seedling foliar N and P concentrations were generally not different between logs and the ground. Growth rates and foliar N concentrations of Quintinia and Weinmannia were greater for
seedlings on tree fern trunks than for seedlings on the ground. Mortality rates did not differ between seedlings on tree
fern trunks and seedlings on the ground. Seedling densities of Quintinia and Weinmannia were greater on logs and tree
ferns than on the ground. Podocarpus densities were not different between logs and the ground, and this species did
not occur on tree ferns. Quintinia and Weinmannia benefit from establishment on elevated microsites but this is not
clearly the case for Podocarpus. Tree regeneration niches for such slow-growing species can only be determined
through long-term studies.
Résumé : Nous avons déterminé si les semis des arbres de la canopée ont des taux de croissance et de mortalité différents sur différents microsites dans les forêts pluviales alpestres de l’ouest de l’île du Sud, en Nouvelle-Zélande. Les taux
de croissance relative en hauteur des semis de trois espèces, Podocarpus hallii, Quintinia acutifolia et Weinmannia racemosa,
étaient très faibles (moyenne = 0,037 cm·cm–1·an–1). Le taux de croissance des semis était plus élevé sur les troncs
d’arbres qu’au sol en pleine lumière, mais la probabilité que les semis sur les troncs d’arbres meurent était aussi plus
élevée en pleine lumière. Les concentrations foliaires de N et de P des semis étaient généralement identiques sur les troncs
d’arbres et au sol. Le taux de croissance et la concentration foliaire de N des semis de Quintinia et de Weinmannia sur
les troncs de fougères arborescentes étaient plus élevés qu’au sol. Le taux de mortalité n’était pas différent sur les troncs
de fougères arborescentes et au sol. La densité des semis de Podocarpus n’était pas différente sur les troncs d’arbres et
au sol et cette espèce était absente des troncs de fougères arborescentes. Quintinia et Weinmannia qui s’établissent sur
des microsites surélevés sont avantagés mais ce n’est pas clairement le cas pour Podocarpus. Les niches de régénération
des arbres pour des espèces à croissance aussi lente peuvent uniquement être déterminées par des études à long terme.
[Traduit par la Rédaction]
Bellingham and Richardson
Introduction
Forest understories are a mosaic of different microsites,
including fallen logs, litter, tip-up mounds, and pits (Harper
1977; Christy and Mack 1984; Christie and Armesto 2003).
Coexistence in species-rich forests can be explained in part
by different tree species regenerating on different microsites
(Grubb 1977; Harmon and Franklin 1989). Fallen logs, in
particular, are a safe site for establishment of many trees,
especially in temperate and boreal forests (Lusk 1995;
Takahashi et al. 2000; Lusk and Kelly 2003), with seedling
densities being much greater on fallen logs than on the
ground (Stewart and Veblen 1982; Christy and Mack 1984).
Received 8 April 2005. Resubmitted 21 August 2005.
Accepted 20 December 2005. Published on the NRC Research
Press Web site at http://cjfr.nrc.ca on 31 March 2006.
P.J. Bellingham1 and S.J. Richardson. Landcare Research,
P.O. Box 69, Lincoln 8152, New Zealand.
1
Corresponding author (e-mail:
bellinghamp@landcareresearch.co.nz).
Can. J. For. Res. 36: 910–918 (2006)
918
Differences in seedling growth and survival in different
microsites should have consequences for community composition (Beckage and Clark 2003). Seedling growth and survival are generally enhanced at high light levels, but individual
species vary in response to increased light (Denslow et al.
1990; Osunkoya et al. 1992; Kobe et al. 1995; Wright et al.
1998). Seedling growth and survival are also variable among
species across microsites (Carlton and Bazzaz 1998); for
some species growth and survival is enhanced on elevated
microsites including logs (Gray and Spies 1997). Reasons
for observed differences include ecological filters that operate more on seedlings in some microsites than those in others. On the forest floor, these filters include deep litter
(Christie and Armesto 2003) and competition from understory
vegetation (Harmon and Franklin 1989; George and Bazzaz
1999; Beckage and Clark 2003); influences of both may be
reduced on elevated microsites. Another reason for enhanced
growth and survival on elevated microsites may be that more
nutrients are available for seedlings on these sites, since they
need not compete with trees, as they do on the ground
(Coomes and Grubb 2000). Since individual species vary in
response to both light and available microsites, it is likely
doi:10.1139/X05-308
© 2006 NRC Canada
Bellingham and Richardson
Fig. 1. Location of the study area in the western South Island,
New Zealand. Plots were located along the transects that are
shown on the map. The intersection of latitude and longitude in
the inset shows the study site location.
that interactions between the two could further enhance
prospects for coexistence. The effects of interactions between light and microsites, especially elevated microsites
such as logs, on seedling growth and survival remain largely
unknown and have been examined over rather short intervals
(1 year; Gray and Spies 1997).
In this study we examined growth and survival of naturally regenerated seedlings of three canopy tree species across
microsites over 6 years in a cool temperate montane forest in
New Zealand. We compared seedling density, growth, and
survival at a catchment scale, on the ground, on logs, and on
tree fern trunks. Although ferns on the forest floor can act as
ecological filters, reducing seedling recruitment (George and
Bazzaz 1999; Coomes et al. 2005), those that develop trunks
may provide safe sites for some species (Pope 1926; Newton
and Healey 1989). Previous studies have shown differences
in seedling density of these species across the three microsites
(Stewart and Veblen 1982; Allen and Rose 1983; Stewart
and Burrows 1989).
In the mosaic of the forest understory, naturally regenerated seedlings that we studied have already been subject to
ecological filters. For example, there are differences in seed
retention and predation between the ground and logs (Christy
and Mack 1984; Harmon and Franklin 1989; Lusk 1995;
LePage et al. 2000). This study addresses ecological filters
that act on seedlings that have established. Growth and survival of established seedlings in a heterogeneous forest understory are critically important in determining which seedlings
ultimately replace the canopy (Grubb 1977; Clark et al. 1999;
Nakashizuka 2001).
911
Methods
Study site
The ca. 10 km2 study site was in the upper reaches of the
Kokatahi River valley, Hokitika River catchment, western
South Island, New Zealand (42°56–42°58′S, 171°12–171°15′E,
320–780 m a.s.l., with surrounding peaks >2000 m a.s.l.,
Fig. 1). The main geological substrate of the area is foliated
schist, grading to semi-schist in the east. The area has a high
rate of geological uplift (>10 mm·year–1) (Whitehouse 1988),
with high rates of erosion and periodic large earthquakes
(Wells et al. 2001). Rainfall is ca. 7000–8000 mm·year–1,
with much occurring as high-intensity events (Henderson
and Thompson 1999). Mean average annual temperature is
ca. 10 °C. Soil development in the valley occurs rapidly with
rapid nutrient loss; nutrient availability peaks at <200 years,
and Podsols can form in as little as 500 years (Tonkin and
Basher 2001). Humaquepts and Endoaquepts are the predominant soils of the valley.
Cool temperate montane rain forests constitute much of
the vegetation of the valley and are dominated by evergreen
angiosperms (Metrosideros umbellata, Weinmannia racemosa,
Quintinia acutifolia, and Griselinia littoralis; nomenclature
follows Allan 1961 except where other authorities are given)
and conifers (principally Podocarpus hallii, Reif and Allen
1988). Landslides and floods are common and give rise to
sites of primary successions, while secondary successions
occur after widespread death of canopy trees, which has occurred throughout the valley since the 1940s (Allen and Rose
1983; Reif and Allen 1988).
Field methods
We sampled the vegetation throughout the valley using
22 permanently marked plots (20 m × 20 m) established
systematically along seven random compass lines (Fig. 1)
(Allen 1993). The origin of each line was located along a
stream channel in a restricted random fashion, and plots
were located at 100 m contour intervals until subalpine shrub
communities were reached. Each line had two to five plots
(mean = 3.1 plots). Lines origins ranged from 300 to 1200 m
apart.
In each plot, circular ground subplots (Table 1) were on
an equally spaced grid. The nearest log ≥5 cm diameter
within 2 m of a ground subplot was identified in 21 plots in
1997; in one plot dominated by early-successional vegetation there were no logs. On each log, a datum closest to the
centre of the ground subplot was selected, and the log subplot area was defined as the upper surface of the log 25 cm
on either side of this datum (Table 1). Logs provided a mean
surface area of 34.1 m2 (range: 3.0–100 m2) per 400 m2 plot.
There were, on average, 17 (range: 5–39) logs per plot, and
30% of all logs were of the canopy tree M. umbellata. Tree
ferns (Cyathea smithii and Dicksonia squarrosa) occurred in
12 plots ≥610 m a.s.l. at a mean density of 25 stems/plot
(range: 3–66 stems/plot). Cylindrical tree fern subplots were
established 25 cm above and below a 135 cm datum (Table 1) on 214 C. smithii trunks and 11 D. squarrosa trunks.
Tree ferns provided an average surface area of 35.0 m2/plot
(range: 3.3–101 m2/plot); this is likely to be an overestimate
of the area that could be colonized because seedlings seldom
© 2006 NRC Canada
912
Can. J. For. Res. Vol. 36, 2006
Table 1. Plot design (means ± SE) and the total numbers of tagged tree seedlings ≥15 cm
tall and ≤135 cm tall tagged in 1997 for measurement of growth and mortality on three
microsites.
Plots (n)
Subplots per plot (n)
Subplot size (m2)
Tagged seedlings per species (n)
Podocarpus hallii
Quintinia acutifolia
Weinmannia racemosa
Ground
Logs
Tree ferns
22
24
0.75
21
20±0.72
0.20±0.010
12
19±4.7
0.28±0.003
32
98
75
9
33
70
0
46
50
establish on the upper trunks of C. smithii, which are covered by retained dead fronds (Page and Brownsey 1986).
Seedlings of three common forest trees, Podocarpus hallii
(Podocarpaceae), Quintinia acutifolia (Grossulariaceae), and
Weinmannia racemosa (Cunoniaceae) (hereafter all species
will be referred to by genus only), ≥15 cm tall and ≤135 cm
tall were tagged, and their heights were recorded in subplots
in February 1997. All three species were tagged in ground
and log subplots, and Quintinia and Weinmannia were
tagged in tree fern trunk subplots; Podocarpus was never
found on tree ferns (Table 1). Height growth and mortality of
tagged seedlings were recorded after 6 years in 2003. Seedling relative height growth rate (RH) was calculated as
[ln(height in 2003) – ln(height in 1997)] / time (6 years)
(George and Bazzaz 1999). There was no evidence of browsing of seedlings by introduced ungulates throughout the study.
We characterized light environments over ground and log
subplots with tagged seedlings in February 2001 using hemispherical photographs taken 1 m above each subplot. Images
were digitized and analyzed using Hemiview version 2.1
(Vieglais and Rich 1997) to determine canopy openness.
There were no major canopy disturbances during the study
that influenced any of the plots (i.e., the maximum loss of
basal area between 1995 and 2002 in any plot was 11%
of initial basal area; P.J. Bellingham, unpublished data). In
ground subplots, we recorded the presence of ferns and (or)
monocot herbs ≥45 cm tall and ≤135 cm tall; the most common of these species were (in descending order) Blechnum discolor, Asplenium gracillimum Col., Cyathea colensoi,
Cyathea smithii, and Microlaena avenacea (Raoul) Hook. f.
We compared leaf nutrient concentrations of 12 randomly
selected seedlings each of Podocarpus, Quintinia, and
Weinmannia ≥30 cm tall and ≤135 cm tall on the ground and
on logs, and of Quintinia and Weinmannia on tree ferns.
Seedlings were collected in February 1999 away from plots
(440–480 m a.s.l.). Foliar N and P were determined from
0.2 g of ground leaf material (including petioles) from each
seedling using automated colorimetric methods (Technicon Instruments 1977).
Mixed model analyses of seedling density, growth rates,
and mortality
All analyses of seedling density, RH, and mortality used
hierarchical mixed models that allowed us to include both
fixed effects (microsite, species, and canopy openness) and
random effects (subplot within plot). Seedling density data
followed a negative binomial distribution and were analyzed
using generalized linear mixed effects models (GLMM) with
penalised quasi-likelihood, a Poisson distribution, a log link,
and an estimated dispersion parameter (Genstat version 6.1;
Payne 2002). Chi-square statistics for each fixed effect were
obtained using sequence-independent Wald tests (Payne 2002).
RH data were analyzed using linear mixed effects (LME)
models in R version 2.1 (Crawley 2005) because the response data followed a normal distribution. Seedling mortality
data were modeled using GLMM with a binomial distribution in R version 2.1. Annual mortality rates (λ) were calculated using the formula in Sheil et al. (1995).
Differences in seedling growth and mortality between the
ground and each elevated microsite (logs and tree ferns)
were tested separately because tree ferns had a limited distribution in the study site and because data on canopy openness were only available for seedlings on the ground and on
logs. First, we tested for the effects of microsite (ground or
log), species (Podocarpus, Quintinia, Weinmannia), and canopy openness using data from 21 plots. Second, we tested
for the effects of microsite (ground or tree fern) and species
(Quintinia and Weinmannia only) using data from the 12
plots where tree ferns occurred.
For analyses of RH and mortality, these regression analyses were used to examine support for a series of candidate
hypotheses. For comparisons of RH and mortality between
the ground and logs, we used all five candidate hypotheses
(Table 2). For comparisons between the ground and tree
ferns, where canopy openness data were not available, we
used a subset of three hypotheses (Table 2). Support for
each candidate model was assessed using the small-sample
Akaike’s information criterion (AICc) and Akaike’s weight
(wi) (Burnham and Anderson 2002).
Data analysis
Seedling foliar nutrient concentration data were arcsin
square-root transformed for analysis. Our analysis design
was unbalanced because Podocarpus was absent from tree
ferns; we therefore tested for the effect of microsite on foliar
N and P concentrations individually within each species using unpaired t tests (Podocarpus) or ANOVA (Quintinia and
Weinmannia).
Results
Ground versus logs
Seedling densities of all three species were greater on logs
than on the ground; this finding was most pronounced for
Weinmannia and least pronounced for Podocarpus (Fig. 2).
The difference was greater still if large ferns and (or) herbs
were present (species × microsite × ferns and (or) herbs in© 2006 NRC Canada
Bellingham and Richardson
913
Table 2. Candidate models for explaining variation in tree seedling growth and mortality between the ground and logs (all candidate
models) and the ground and tree ferns (models with an asterisk) in a New Zealand montane rain forest.
Model
Hypothesis
Null*
Canopy openness
Microsite*
Canopy openness × microsite
Growth and mortality are unrelated to light or microsite.
Light determines growth and survival (Denslow et al. 1990; Kobe et al. 1995).
Elevated microsites are more favourable for growth and survival (Gray and Spies 1997).
There will be a positive interaction between high light levels and favourable microsites on growth
and survival (Gray and Spies 1997; Carlton and Bazzaz 1998).
Species-specific effects will interact with microsites to promote coexistence (Lusk 1995; Carlton and
Bazzaz 1998; Christie and Armesto 2003).
Species × microsite*
Fig. 2. Density (mean ± 1 SE) of seedlings ≥15 cm tall and
≤135 cm tall of three trees: Podocarpus hallii, Quintinia
acutifolia, and Weinmannia racemosa on logs and the ground:
(a) where ferns and (or) herbs ≥45 cm tall and ≤135 cm tall
were absent and (b) where they were present.
2.0
(a)
1.2
Ground
Log
1.0
0.5
Ground
Log
Tree fern
1.0
Foliar N (%)
1.5
Seedling density (no.·m–2)
Fig. 3. Foliar N and P concentrations (mean ± 1 SE) of seedlings ≥30 cm tall and ≤135 cm tall of three canopy tree species
on the ground, logs, and tree ferns (Podocarpus was not found
on tree ferns). Attributes are not different between microsites if
they share the same letter (t test for comparisons between two
microsites; Tukey test after ANOVA for comparisons between
three microsites, P < 0.05).
0.8
a
b b
b
a
ab
b
a
0.6
0.4
0.2
0.0
(b)
0.0
1.5
0.16
b
1.0
Foliar P (%)
0.12
0.5
0.0
Podocarpus Quintinia Weinmannia
a
a
0.08
0.04
Species
0.00
teraction term, χ[22] = 8.98, P = 0.011; Fig. 2b). Quintinia
seedlings on logs had 18% greater foliar N concentrations
than those on the ground (F[2,33] = 7.11, P = 0.003), whereas
Podocarpus seedlings on logs had 8% lower concentrations
than those on the ground (t[22] = 2.15; P = 0.042; Fig. 3a).
Seedling foliar P concentrations were not different between
logs and the ground for any species.
Seedling growth rates (RH) of Podocarpus, Quintinia, and
Weinmannia were very low, even in sites with high canopy
openness (Fig. 4). A model that included an interaction be-
Podocarpus Quintinia Weinmannia
Species
tween canopy openness and microsite had the greatest support (Table 3). RH on logs increased with canopy openness
but RH on the ground did not (Fig. 4). A model that included
canopy openness alone also had substantial support.
Seedling mortality rates across all species on the ground
and logs were low (2.7%·year–1). Models explaining the
variation in seedling mortality between the ground and logs
© 2006 NRC Canada
914
Can. J. For. Res. Vol. 36, 2006
Fig. 4. Relationship between canopy openness and relative height
growth rate (RH) for seedlings of Podocarpus hallii, Quintinia
acutifolia, and Weinmannia racemosa on the ground (!; solid
line) and on logs (; broken line).
Fig. 5. Mortality in relation to canopy openness for Podocarpus
hallii, Quintinia acutifolia, and Weinmannia racemosa seedlings
on the ground (solid line) and on logs (broken line).
0.4
RH (cm·cm–1·year –1)
0.3
0.2
Logs
0.1
0.0
Ground
-0.1
-0.2
-0.3
-0.4
0
5
10
15
Canopy openness (%)
Table 3. Comparison of candidate models predicting variation in
relative height growth rate (RH) between the ground and logs in
Podocarpus, Quintinia, and Weinmannia in a New Zealand
montane rain forest.
Model
K
AICc
∆i
wi
Canopy openness × microsite*
Canopy openness*
Microsite
Null
Species × microsite
6
4
4
5
8
–778.4
–776.8
–765.4
–762.4
–758.2
0.0
1.6
13.1
16.0
20.2
0.69
0.31
0.00
0.00
0.00
Note: K is the number of model parameters, AICc is the small-sample
Akaike’s information criterion, ∆ i is the difference in AICc between the
best model and each other model, and wi is Akaike’s weight. Models with
∆ i ≤ 2 have substantial support (Burnham and Anderson 2002) and are denoted by an asterisk.
Table 4. Comparison of candidate models predicting variation in
mortality between the ground and logs in Podocarpus, Quintinia,
and Weinmannia in a New Zealand montane rain forest.
Model
K
AICc
∆i
wi
Canopy openness*
Canopy openness × microsite*
Null
Microsite
Species × microsite
3
5
2
3
7
268.5
269.2
270.7
271.4
279.4
0.0
0.8
2.2
2.9
10.9
0.45
0.30
0.15
0.10
0.00
Note: K is the number of model parameters, AICc is the small-sample
Akaike’s information criterion, ∆ i is the difference in AICc between the
best model and each other model, and wi is Akaike’s weight. Models with
∆ i ≤ 2 have substantial support (Burnham and Anderson 2002) and are denoted by an asterisk.
that included canopy openness had the strongest support
(Table 4); seedlings were more likely to die in sites with low
canopy openness (Fig. 5). A model that included canopy
openness alone had stronger support than one that contained
an interaction term between canopy openness and microsite.
Ground versus tree ferns
Seedling densities of Quintinia and Weinmannia on tree
ferns were twice as great as those on the ground (χ[21] = 4.85,
P = 0.028; Fig. 6a). Seedling foliar N concentrations of
Quintinia and Weinmannia were greater on tree ferns than
on the ground (respectively 13% greater, F[2,33] = 7.11, P =
0.003 and 23% greater, F[2,32] = 16.03, P < 0.001; Fig. 3a).
Weinmannia seedling foliar P concentrations were also 18%
greater on tree ferns than on the ground (F[2,32] = 13.92, P <
0.001; Fig. 3b).
Seedling RH on the ground and tree ferns was influenced
by an interaction term between species and microsite, and
the model that included this term had the greatest support
(Fig. 6b; Table 5). Seedling mortality rates of Quintinia and
Weinmannia on the ground and tree ferns were low
(2.7%·year–1). A null model of seedling mortality had the
greatest support (Table 6) but a model containing microsite
had substantial support (Table 6).
Discussion
Preferential colonization of logs and tree ferns
Logs form an important part of the matrix of the forest
floor and understory in this temperate montane rain forest.
They can occupy up to 25% of the understory area, a value
that is comparable to that of other temperate rain forests
(Christy and Mack 1984; Lusk 1995), and they are an important microsite for regeneration. Tree fern trunks also provide a
locally important regeneration microsite at lower altitudes.
Seedling densities of two common canopy tree species, Q.
acutifolia and W. racemosa, were greater on logs or tree fern
© 2006 NRC Canada
Bellingham and Richardson
915
Fig. 6. Seedling (a) densities and (b) relative height growth rate
(RH) of Quintinia acutifolia and Weinmannia racemosa on the
ground and on tree ferns.
Seedling density (no.·m–2)
1.0
(a)
0.8
0.4
0.2
K
AICc
∆i
wi
Null*
Microsite*
Species × microsite
2
3
5
124.6
126.6
129.1
0.0
2.0
4.5
0.68
0.25
0.07
Weinmannia species (Weinmannia trichosperma) has also
been shown in Chilean rain forests (Lusk 1995; Christie and
Armesto 2003), and the importance of tree ferns as a microsite
for establishment of W. racemosa has been shown in other
New Zealand studies (Pope 1926; Wardle 1980; Coomes
et al. 2005). Podocarpus hallii, a canopy tree with larger
animal-dispersed seeds, had similar seedling densities on
logs and on the ground and did not colonize tree ferns. Seedling densities of all three species on the ground were reduced
when large herbs and (or) ferns were present as ground cover,
a findings that is consistent with those of other studies
(George and Bazzaz 1999); in these sites logs and tree fern
trunks provide an especially important site for seedlings to
establish (June and Ogden 1975; Coomes et al. 2005).
0.0
RH (cm·cm –1·year –1)
Model
Note: K is the number of model parameters, AICc is the smallsample Akaike’s information criterion, ∆ i is the difference in AICc
between the best model and each other model, and wi is Akaike’s
weight. Models with ∆ i ≤ 2 have substantial support (Burnham and
Anderson 2002) and are denoted by an asterisk.
0.6
0.10
Table 6. Comparison of candidate models predicting variation
in mortality between the ground and tree ferns in Quintinia
and Weinmannia in a New Zealand montane rain forest.
(b)
0.08
Quintinia
Weinmannia
0.06
0.04
0.02
0.00
Ground
Tree fern
Microsite
Table 5. Comparison of candidate models predicting variation in relative height growth rate (RH) between the ground
and tree ferns in Quintinia and Weinmannia in a New Zealand montane rain forest.
Model
K
AICc
∆i
wi
Species × microsite*
Microsite
Null
6
4
3
–256.4
–252.4
–242.8
0.0
4.0
13.5
0.88
0.12
0.00
Note: K is the number of model parameters, AICc is the smallsample Akaike’s information criterion, ∆ i is the difference in AICc
between the best model and each other model, and wi is Akaike’s
weight. Models with ∆ i ≤ 2 have substantial support (Burnham and
Anderson 2002) and are denoted by an asterisk.
trunks than on the ground. Both species have small winddispersed seeds, which may be unable to penetrate or germinate beneath the litter layer on the ground (Metcalfe et al.
1998; Christie and Armesto 2003). We did not measure microsites on the ground where small-seeded species established,
but other studies have shown that at least Weinmannia preferentially colonizes exposed subsoil and steep microslopes
(Beveridge 1973). Impediments to colonization such as a
litter layer are reduced on logs and tree fern trunks. Disproportionate colonization of logs by another small-seeded
Costs and benefits of colonization of elevated microsites
Most seedlings in this forest scarcely grew in height even
when light levels were high, irrespective of microsite
(Fig. 4) (cf. Beckage and Clark 2003). Indeed, among the
186 seedlings tagged in this forest in 1980 on the ground
and <135 cm tall, no Podocarpus and only 10% of Quintinia
and Weinmannia seedlings grew to be >135 cm in 23 years
(P.J. Bellingham and R.B. Allen, unpublished data). Longpersistent seedlings with low growth rates (“oskars” sensu
Silvertown 1987) are characteristic of many trees in temperate and tropical forests, and in our study three canopy species had low and often zero or negative growth rates and low
mortality, both on logs and on the ground. Oskars can respond to increased light levels even after long periods in
shaded understories (e.g., Wilson and Fischer 1977). A benefit of establishment on logs was that at high light levels
seedlings had slightly increased growth rates, whereas those
on the ground did not. Superior growth at higher light levels
among seedlings on logs could be due to less intense root
competition for nutrients, as predicted by Coomes and
Grubb (2000). If this were so, we would expect there to be
higher foliar nutrient levels in seedlings on logs. Instead
there were either no differences or inconsistent trends in
seedling foliar N and P between logs and the ground, and
concentrations were low (Fig. 3), as has been shown for
seedlings from nutrient-poor tropical forest soils (e.g., Lewis
and Tanner 2000). That seedlings on logs had generally no
greater foliar N and P concentrations than seedlings on the
ground is probably due to the low concentrations of N and P
in decaying logs (e.g., Takahashi et al. 2000). Another explanation for superior growth at higher light levels among seedlings on logs is that these seedlings on elevated microsites
© 2006 NRC Canada
916
occur above the fern and large herb filter that occurs commonly on the ground in these forests. Since species that
commonly constitute this fern and herb layer are especially
responsive to high light levels and nutrients (Coomes et al.
2005), increases in their biomass at high light levels may
disadvantage seedlings on the ground. Further investigations
are needed to determine effects of above- and below-ground
competition on seedling growth between microsites. Experiments that manipulate the fern and herb layer, coupled with
trenching, could determine reasons for lower growth rates of
seedlings on the ground at high light levels.
The chief cost of seedling establishment on logs was mortality. There was a higher probability of seedling mortality
on logs than on the ground in all but the lowest light environments (Fig. 5). Studies in western North America have
found higher survival of seedlings on logs than on the ground
(DeLong et al. 1997; Gray and Spies 1997) but we found the
opposite. This may be because mortality was evaluated over
1 year in the North American studies compared with 6 years
in our study. The causes of higher mortality on logs in our
study are unknown, but a reason could be that higher seedling densities result in greater competition and hence greater
mortality. Logs are also prone to movement or destruction
more frequently than terrestrial habitats (Harmon 1989).
There are benefits and no apparent costs for seedlings of
the small-seeded species Quintinia and Weinmannia that establish on tree fern trucks. Tree ferns also cast deep shade on
the forest floor and reduce opportunities for seedling establishment and growth on the ground (Coomes et al. 2005), so
another benefit of establishment on tree fern trunks may derive from reduced numbers of seedlings on the forest floor
and hence reduced competition during onward growth. RH,
foliar N concentrations, and, in the case of Weinmannia, foliar P concentrations were greater for seedlings that establish
on tree fern trunks than for those on the ground, and mortality was not different between the two microsites. Investigations are required to determine whether the fibrous trunk
exterior or stemflow from suspended humus at the stipe bases
is the source of enhanced seedling nutrition (Fig. 3) and to
determine how light, which we did not measure on tree fern
trunks, affects seedling growth.
Links to canopy dynamics
There is widespread death of the dominant canopy trees
Podocarpus and Weinmannia as well as of another canopy
dominant, Metrosideros umbellata, at scales of tens of hectares in many South Island montane rain forests (Allen and
Rose 1983; Reif and Allen 1988). After canopy dieback,
large numbers of fallen logs provide regeneration microsites
for some canopy tree species. Similarly, tree ferns, which regenerate after canopy dieback, provide additional regeneration microsites in these forests (Wardle 1980). Other studies
(e.g., Cornett et al. 1997) have described a feedback between
canopy trees and provision of microsites for their
regeneration. There is some evidence of such a feedback in
South Island montane rain forests. Recruitment of Weinmannia in these forests (0.9%·year–1; trees >10 cm DBH over
23 years) nearly offset its mortality (1.0%·year–1; Bellingham et al. 1999). Weinmannia seedlings, as well as Quintinia seedlings, had disproportionately high density on logs
and grew rapidly on tree fern trunks. Verification of a feed-
Can. J. For. Res. Vol. 36, 2006
back depends on further measurement of tagged seedlings on
different microsites to determine whether these slow-growing
seedlings survive to become trees. Moreover, a feedback does
not apply generally. Podocarpus established as seedlings on
logs and the ground but their growth rates were very slow
and probably inadequate to replace a dying canopy (nil recruitment and 3%·year–1 mortality of Podocarpus trees
>10 cm DBH over 23 years; Bellingham et al. 1999).
Metrosideros umbellata is often a dominant canopy tree in
this forest that contributed the largest proportion of logs, and
these decompose very slowly (Coomes et al. 2002), providing an important site for regeneration. Like Quintinia and
Weinmannia, M. umbellata is small seeded and wind dispersed, yet in these forests it seldom regenerated on logs and
very rarely on the ground or on tree ferns (Stewart and
Veblen 1982; Allen and Rose 1983). Thus it is not a major
component of regeneration after death of former canopies;
this contrasts with the regeneration ecology of Metrosideros
polymorpha after canopy death in Hawaii (Jacobi et al. 1983).
Both Podocarpus and M. umbellata probably depend principally on primary seres for their regeneration in these
montane rain forests (Stewart and Veblen 1982; Wells et al.
2001). Currently, however, secondary succession is widespread in these forests after canopy death. The established
seedling bank may diminish the importance of new germinants during secondary succession, and hence even slowgrowing established seedlings might ultimately replace the
canopy. More investigations over long periods are needed to
determine the importance of seedling banks in forest regeneration.
Acknowledgements
L.E. Burrows, L. Broad, and others initially established
plots under the direction of I.L. James. Plot data from derives from the National Vegetation Survey databank. M.E.
Brignall-Theyer, S.J. Ferriss, C.H. Lusk, M. McKay, C.W.
Morse, J.M. Steven, P.A. Suisted, D.A. Wardle, and D.K.
Zanders assisted in field and lab measurements. P.A. Townsend
digitized and analyzed hemispherical photographs. B.K. Daly
conducted foliar nutrient analyses. G. Forrester and R.P.
Duncan provided statistical advice. R.B. Allen, C. Bezar,
C.D. Canham, D.A. Coomes, P.J. Grubb, C.H. Lusk, M.S.
McGlone, and D.A. Peltzer provided critical comments on
the manuscript. The research was supported by the New
Zealand Foundation for Research, Science and Technology
contract C09X0206.
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