Ecology, 92(9), 2011, pp. 1828–1838
Ó 2011 by the Ecological Society of America
Seedling growth responses to soil resources in the understory
of a wet tropical forest
ELLEN K. HOLSTE,1,3 RICHARD K. KOBE,1
2
AND
CORINE F. VRIESENDORP2
1
Michigan State University, Department of Forestry, 126 Natural Resources, East Lansing, Michigan 48824 USA
Environment, Culture, and Conservation, The Field Museum of Natural History, 1400 South Lake Shore Drive, Chicago,
Illinois 60605 USA
Abstract. Plant growth responses to resources may be an important mechanism that
influences species’ distributions, coexistence, and community structure. Irradiance is
considered the most important resource for seedling growth in the understory of wet tropical
forests, but multiple soil nutrients and species have yet to be examined simultaneously with
irradiance under field conditions. To identify potentially limiting resources, we modeled tree
seedling growth as a function of irradiance and soil nutrients across five sites, spanning a soil
fertility gradient in old-growth, wet tropical forests at La Selva Biological Station, Costa Rica.
We measured an array of soil nutrients including total nitrogen (total N), inorganic N (nitrate
[NO3] and ammonium [NH4þ]), phosphate (PO4 ), and sum of base cations (SBC; potassium,
magnesium, and calcium). Shade in the forest understory did not preclude seedling growth
correlations with soil nutrients. Irradiance was a significant predictor of growth in 52% of the
species, inorganic N in 54% (NO3 in 32%; NH4þ in 34%), total N in 47%, SBC in 39%, and
PO4 in 29%. Overall, growth was correlated with both irradiance and soil nutrients in 45% of
species and with soil nutrients only in an additional 48%; rarely was irradiance alone
correlated with growth. Contrary to expectations, the magnitudes of growth effects, assessed
as the maximum growth response to significant resources for each species, were similar for
irradiance and most soil nutrients. Among species whose growth correlated with soil nutrients,
the rank importance of nutrient effects was SBC, followed by N (total N, NO3, and/or NH4þ)
and PO4. Species’ growth responsiveness (i.e., magnitudes of effect) to irradiance and soil
nutrients was negatively correlated with species’ shade tolerance (survival under 1% full sun).
In this broad survey of species and resources, the nearly ubiquitous effects of soil nutrients on
seedling growth challenge the idea that soil nutrients are less important than irradiance in the
light-limited understory of wet tropical forests.
Key words: forest understory; irradiance; La Selva Biological Station, Costa Rica; neotropics; plant
growth; seedlings; shade tolerance; soil nutrients; wet tropical forest.
INTRODUCTION
Tropical forest understories are spatially heterogeneous in irradiance (Nicotra et al. 1999) and soil
resources (E. K. Holste et al., unpublished manuscript),
and species-specific seedling growth and survivorship
responses to resource levels could influence community
structure. In both temperate and tropical forests, there is
an interspecific trade-off between survivorship under
low light (i.e., shade-tolerant species) vs. growth under
high light (i.e., light-demanding species) that could
promote species coexistence across light gradients (Kobe
et al. 1995, Kobe 1999). Similarly, interspecific trade-offs
between growth and survivorship exist along edaphic
gradients, potentially contributing to species’ distributions (Schreeg et al. 2005, Russo et al. 2008). These
resource-based trade-offs could be a mechanism for
Manuscript received 30 August 2010; revised 31 January
2011, Accepted 30 March 2011; final version received 3 May
2011. Corresponding Editor: K. D. Woods.
3 E-mail: [email protected]
resource partitioning (Grubb 1977), which could sustain
tree species diversity in tropical forests. Therefore,
understanding species-specific seedling growth responses
to resources may be crucial for predicting forest
dynamics.
In tropical forests, irradiance is considered to be ‘‘the
single most limiting resource’’ (Pearcy 2007), with
sometimes ,1% of above canopy radiation transmitted
to the forest floor (Chazdon and Fetcher 1984). Wet
tropical forest seedlings exhibit both intra- and interspecific variation in growth to differing light levels
(Augspurger 1984, Poorter 1999). Even in low-light
environments, such as beneath closed canopy forests,
tropical seedling growth varies interspecifically in
response to light availability (Montgomery and Chazdon 2002).
Soil nutrients also can influence tree seedling growth
(Burslem et al. 1995, Dent and Burslem 2009). In
tropical forests, species differ in the direction and
strength of growth responses to soil factors (Baraloto
et al. 2006). Phosphorus (P) is widely thought to be
1828
September 2011
SEEDLING RESPONSES TO SOIL RESOURCES
more limiting than nitrogen (N) in lowland tropical
forests because most tropical soils are N rich relative to
other nutrients (Hedin et al. 2009). Seedling growth
responses to P additions support limitation by P
(Lawrence 2001, Ceccon et al. 2003). Yet, N also could
alleviate P limitations by providing a substrate to
construct extracellular phosphatases to acquire P
(Treseder and Vitousek 2001). Based on reviews of
plant–soil relations in lowland wet tropical forests,
Sollins (1998) proposed the rank order of nutrients
most strongly influencing species’ composition, and by
extension seedling performance, are P, base cations
(potassium, calcium, magnesium), and N.
Soil nutrients may interact with irradiance to influence
tree seedling performance (e.g., Kobe 2006). A common
assumption is that light-demanding species invest more
in traits that maximize growth (Herms and Mattson
1992) since they tend to have small seeds, small initial
seedling size, and photosynthetic cotyledons (Kitajima
2002). In contrast, shade-tolerant species have larger
seeds, storage cotyledons, larger initial seedling height
and mass, and invest in functions that improve
survivorship such as defense against natural enemies
(Coley and Barone 1996) and carbohydrate storage
(Myers and Kitajima 2007). The growth of both lightdemanding and shade-tolerant seedlings respond to soil
nutrients under high-light availability (reviewed by
Lawrence 2003), likely because faster growth increases
demand for nutrients (Peace and Grubb 1982). Seedlings
in the shaded understory also could benefit from
increased soil nutrient availability via improved light
capture (Fahey et al. 1998). Soil nutrients can influence
light-demanding and shade-tolerant seedling growth in
the forest understory (Yavitt and Wright 2008, Palow
and Oberbauer 2009), yet shade-tolerant species presumably have a lower nutrient demand due to their
cotyledon reserves and slower growth. Thus, we expect
seedling growth of light-demanding species to be more
dependent upon soil resources than more shade-tolerant
species. Furthermore, seedling dependency on external
sources generally develops earlier for light than mineral
nutrients, suggesting greater importance of light than
soil nutrients during early seedling establishment (Kitajima 2002). Thus, we expect growth–irradiance correlations to be more prevalent and irradiance to have a
greater effect than soil nutrients on seedling growth in
the shaded forest understory.
In this study, we examined the growth responses of 94
species of woody seedlings (represented by 12 800
individuals) to irradiance and soil nutrients under field
conditions to better understand species-specific seedling
performance and implications for forest dynamics. We
hypothesized that: H1, Irradiance limitations to seedling
growth are more prevalent among species and are of a
greater magnitude than soil resource limitations to
seedling growth; H2, Among the species whose seedling
growth is sensitive to soil nutrients, the rank importance
of soil nutrients is (in decreasing order) P, base cations,
1829
and N; and H3, Across species, the effect of irradiance
and soil nutrients on seedling growth is negatively
correlated with shade tolerance.
METHODS
Site description
The study took place in five sites in mainly old-growth
wet tropical forest at La Selva Biological Station, Costa
Rica. A portion of 1 site contained secondary forest,
which was associated with higher wood productivity
(T. W. Baribault, personal communication), but not
higher seedling growth. La Selva is located in the
Atlantic lowlands at the Sarapiqui and Puerto Viejo
rivers’ convergence (10826 0 N, 84800 0 W) and receives
mean annual rainfall of 4367 mm (mean monthly
minimum of 124 mm). La Selva soils span a fertility
gradient from relatively fertile entisols and inceptisols of
alluvial origin to low fertility ultisols developed on old
lava flows (McDade and Hartshorn 1994); sites were
established on three volcanic and two alluvial soils. Each
site was centered on a transect of 200 contiguous 1-m2
quadrats. In each transect, seedlings were identified and
height measurements taken every six weeks from
February 2000 to September 2009.
Resource measurements
We measured light and soil nutrient availability for
each 1-m2 quadrat, which is an appropriate spatial scale
to assess seedling resource availability (E. K. Holste et
al., unpublished manuscript). Light availability was
measured with hemispherical canopy photos six times
during the course of the study. We also measured a
broad suite of soil characteristics for each quadrat (three
composited subsamples per 1-m2 quadrat), including
inorganic nitrogen (nitrate [NO3] and ammonium
[NH4þ]), total nitrogen (total N), phosphate (PO4 ),
potassium (Kþ), calcium (Caþ), and magnesium (Mgþ).
Extractable Kþ, Caþ, and Mgþ were highly correlated
and were combined into a composite metric of sum of
base cations expressed in charge equivalents (SBC).
However, total N, NO3, and NH4þ were not strongly
correlated, so all N forms were examined individually.
Detailed methods for resource measurements are presented in Appendix A.
Data analyses
Across the five sites, the data set encompassed 522
woody species (including lianas and canopy, subcanopy,
and understory trees) and 14 000 individuals. With the
aid of a database compiled by C. F. Vriesendorp
(available online),4 we identified all seedlings to species
(89% of individuals) or morphospecies. Any misidentified seedlings would be a small percentage of the total
sample. Among the 522 potential species, only 95 species
had sample sizes 20 individuals (represented by
4
hhttp://fm1.fieldmuseum.org/seedlings/index.phpi
1830
ELLEN K. HOLSTE ET AL.
;12 800 individuals); one species was excluded from
analyses because all individuals were found in only two
quadrats. Seedlings were included if they were alive for
at least two censuses so that height growth over an
interval could be calculated (i.e., DHeight ¼ Heightfinal Heightinitial).
Measurements of final height were truncated at
September 2009, the last available seedling census.
Because a decrease in seedling height can signal the
start of the death process (and often was), we
determined final height as the last census at which
DHeight for the most recent interval was zero or
positive. Seedling life span was calculated as the time
(in months) between final height and initial height. The
growth of a seedling for a particular species can be
characterized as a compound interest formula:
h
Heightfinal ¼ Heightinitial ð1 þ RÞlife span þ e ; Nð0; r2 Þ
where R is the growth rate and is specified as a linear
function of resources (irradiance, NO3, NH4þ, total N,
PO4, and/or SBC), h accounts for changes in the
compounding of growth with seedling age, and e is
normally distributed error with variance r2, estimated as
a parameter from the data. The compounding of
seedling growth may slow over time due to exhaustion
of seed reserves, the accumulation of respiring nonphotosynthetic tissue, or cumulative effects of natural
enemies such as pathogens or herbivores. When h ¼ 1,
compounding of growth is constant over seedlings of
different life spans within the same species; h , 1
indicates a diminishing, while h . 1 indicates increasing
compounding of growth for longer lived seedlings. We
expected growth rate (R) to increase with increasing
irradiance and soil resources. Seedling growth often is
asymptotically related to irradiance, especially across
broad ranges of irradiance (e.g., Pacala et al. 1994, Kobe
2006). However, the range of canopy openness encountered in this study was limited (0% to 6.72%), so we used
linear models to characterize the relationship between
growth and irradiance.
Nonlinear models were fit using maximum likelihood
in R project computing software (R package nlme;
Pinheiro et al. 2011). The best species’ models were
chosen based upon (1) lowest Akaike’s information
criterion (AIC) with a minimum AIC difference of at
least two, (2) parameter estimates that were significantly
different from zero (or unity for h), and (3) model fit as
assessed by r 2 values (calculated as the square of the
Pearson correlation coefficient between observed and
predicted final heights). For each species, 10% of the
seedlings were randomly selected as a holdout set (i.e.,
not used for model calibration) for model validation.
For each species, the best fit model was used to predict
final height for holdout set seedlings, and r 2 values were
calculated.
In general, seedlings of a given species were broadly
distributed across transects and quadrats (also see Kobe
Ecology, Vol. 92, No. 9
and Vriesendorp 2009). Nevertheless, because seedlings
were sampled in belt transects, we tested for spatial
dependence in residual growth for each species transect
with semivariograms. For most species, the lowest
semivariance occurred at a lag distance other than zero,
meaning that seedlings located in the same plot or in
close proximity were not more similar in residual growth
variance than seedlings located farther away (see
Appendix B). For species with some spatial dependency,
confidence intervals on parameter estimates could be
broader. The lack of spatial structure in most residual
growth likely was due to the generally good fit of the
models in which spatial variation in growth was
accounted for in our resource measurements and
models. Thus, seedlings were treated as independent
units within a species.
To express resource effects on a comparable scale,
potential influence of a resource was calculated as a
product of the maximum observed resource level for a
species and corresponding resource parameter estimate
for that species, which was scaled by the mean initial
height across all seedlings to express effects in terms of
height growth (in millimeters) per month. The absolute
value of each maximum effect was compared across
resources. To estimate the rank importance of soil
nutrients and compare their effects on seedling growth
with irradiance, resources effects were considered
significantly different (P 0.05) when their maximum
effects had 29% overlap in their 95% confidence
intervals (Austin and Hux 2002). We compared resource
ranges with significant and nonsignificant species’
responses to determine if the ranges influenced whether
those resources were empirically supported.
We used correlation analysis to test for relationships
among growth responsiveness to resources, shade
tolerance, and seed/initial seedling size. We characterized species’ shade tolerance as the probability of
seedling survival at 1% full sun and zero conspecific
seedling density, calculated from mortality models
developed from the same sites (Kobe and Vriesendorp
2011; R. K. Kobe and C. F. Vriesendorp, unpublished
data); survival at 1% full sun includes both background
and shade-induced mortality and thus differs slightly
from the definition of shade tolerance in Kobe and
Vriesendorp (2011). We obtained seed sizes for 31
species from the KEW Seed Information Database
(http://data.kew.org/sid/sidsearch.html). Mean initial
seedling height for each species was calculated from
our field data. To assess negative density dependence
(Janzen 1970, Connell 1971), we tested for effects of
both con- and heterospecific seedling density on species’
growth by comparing those densities against species’
residual growth.
RESULTS
Summary
In this broad survey of species and resources, we
found support for both soil nutrients and irradiance
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SEEDLING RESPONSES TO SOIL RESOURCES
1831
FIG. 1. Model fit of representative species at La Selva Biological Station, Costa Rica, as assessed by r 2 values for (A) Hampea
appendiculata, r 2 ¼ 0.89; (B) Colubrina spinosa, r 2 ¼ 0.49; (C) Heteropterys laurifolia, r 2 ¼ 0.85; (D) Aegiphila sp., r 2 ¼ 0.82; (E)
Virola koschnyi, r 2 ¼ 0.65; and (F) Psychotria sp. 3, r 2 ¼ 0.58. Dashed and solid lines represent 95% confidence intervals and
prediction intervals, respectively.
effects on seedling growth in a wet tropical forest
understory (Appendix C). Across all species, a mean of
58% of the variation in growth (median r 2 ¼ 0.70) was
explained by simple size- and resource-based growth
models (e.g., Fig. 1). On average, resources explained
;25% of the variation in growth within species (mean of
differences in r 2 values between models containing initial
height and resources vs. only initial height) and initial
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ELLEN K. HOLSTE ET AL.
Ecology, Vol. 92, No. 9
FIG. 2. Percentage of species for which each resource was correlated with growth. SBC is the sum of base cations (potassium,
magnesium, and calcium).
height ;33% of growth variation. The holdout data set
provided strong validation of the growth models (mean
r 2 ¼ 0.69 across species). Of the 94 species with 20
individuals (and sufficient variation in growth and
resources), three species had several single-resource
models that contained significant parameters with
similar AIC support and r 2 values. Growth of two
species was influenced by outliers, and influential
outlying points were eliminated in subsequent analyses.
While con- and hetero-specific density influenced survivorship in related studies (e.g., McCarthy-Neumann and
Kobe 2010, Kobe and Vriesendorp 2011), they were not
correlated with growth in this study (residual growth vs.
conspecific density, mean r 2 ¼ 0.013, vs. heterospecific
density, mean r 2 ¼ 0.010). Thus, con- and hetero-specific
density may largely influence seedling survivorship, but
not growth, and are not considered further.
Soil resources and irradiance influenced seedling growth
Contrary to expectation, irradiance was not the most
prevalent or strongest correlate of seedling growth. With
regard to prevalence, growth of 48% of the species was
correlated with only soil nutrients, and growth of an
additional 45% of species was related to both soil
nutrients and irradiance (see Appendix C). In 7% of
species, growth was correlated with only irradiance.
Among soil nutrients, inorganic N (NO3 and/or NH4þ)
was a significant predictor of growth in over half (54%)
of the species (NO3 in 32%, and NH4þ in 34%), total N
in 47% of the species, and SBC in 39% of species.
Phosphate, typically assumed to be the most limiting
nutrient in tropical systems, was least prevalent as a
correlate of growth (29%). The range of resources for
each species did not influence whether that factor was
empirically supported, as resource ranges did not differ
for significant and nonsignificant species responses (for
irradiance, z ¼ 1.47, P ¼ 0.14; for NO3, z ¼ 1.11, P ¼
0.27; for NH4þ, z ¼ 0.80, P ¼ 0.42; for PO4, z ¼ 0.25, P ¼
0.81; for SBC, z ¼0.40, P ¼ 0.69), with the exception of
total N (z ¼ 2.13, P ¼ 0.03). Positive growth–resource
correlations occurred in 45% of species for irradiance,
38% for total N, 30% for SBC, 23% and 22% for NO3
and NH4þ, respectively, and 18% for PO4; approximately 6–12% of species’ resource–growth relationships
were negative, but not necessarily negative within the
same species (Fig. 2).
Contrary to expectation, most soil nutrients (with the
exception of NO3, t ¼ 3.07, df ¼ 130.55, P ¼ 0.003) had
similar magnitudes of effect on seedling growth as
irradiance (Figs. 3 and 4). Across the range of measured
resources among species, irradiance’s mean potential
effect on growth was 4.30 mm/month. Mean potential
magnitudes of effect for soil nutrients were 4.62 mm/
month for total N, 2.66 mm/month for SBC, 2.33 mm/
month for PO4, 2.42 mm/month for NH4þ, and 1.69
mm/month for NO3 (see Appendix D). Among species
for which both irradiance and a soil nutrient were
correlated with growth, irradiance had a greater effect
on growth in about half of the species, whereas the
effects of a soil nutrient were greater than or comparable
to irradiance in the other half (Table 1, Fig. 4A–C).
Among species for which growth was correlated with
only soil nutrients and not irradiance, the rank
importance of nutrients was first SBC, followed by N
(Total N, NO3, and/or NH4þ) and PO4. SBC effects
on magnitude of growth response were greater than total
N in 42% of species, greater than PO4 and NO3 in
47%, and greater than NH4þ in 59%; other nutrients had
the strongest magnitudes of effect in fewer cases (Table
2).
Life span effects on compounding of growth
Of the 94 species, 24 species (27%) experienced
diminishing compounding of growth (h , 1), and 7
species (8%) experienced accelerating growth (h . 1)
with increasing life span. Species estimates of h were
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SEEDLING RESPONSES TO SOIL RESOURCES
1833
FIG. 3. Mean absolute values of resource effects on seedling growth across species. Error bars denote standard error; letters
represent significantly different pairwise comparisons at P ¼ 0.05. Resource effects are scaled by mean initial seedling height to
express responses in units of height growth.
weakly correlated with initial seedling size (F1,92 ¼ 4.36,
P ¼ 0.04, r ¼ 0.21), but not shade tolerance (F1,89 ¼ 0.47,
P ¼ 0.49, r ¼ 0.07).
Species growth responses to resources covaried
with shade tolerance
Across species, seed size was strongly correlated with
mean initial seedling height (F1,31 ¼ 50.17, P , 0.001, r ¼
0.79). Since we had seed size for only one-third of
species, we used species mean initial height as a
surrogate for seed size. As expected, initial seedling
height and shade tolerance (i.e., low-light survival) were
positively correlated across species (F1,89 ¼ 21.66, P ,
0.001, r ¼ 0.44).
Across species, magnitude of growth responses to
resources were negatively correlated with low-light
survival, but not with initial seedling size, with the
exception that the growth effects of NO3 decreased
with seedling size (Appendix E). Low-light survival was
negatively correlated with growth responses to irradiance, SBC, NO3, NH4þ, and PO4 (Fig. 5A–E).
Growth responses to total N were similar for lightdemanding and shade-tolerant species (Fig. 5F).
DISCUSSION
In wet tropical forest understories, both irradiance
and seedling growth rates are generally very low (Clark
and Clark 1992). Despite low light levels, this study
highlights the potential importance of both irradiance
and soil nutrients to tropical seedling growth (as
proposed by Coomes and Grubb 2000) and suggests
that growth by light-demanding species created a higher
demand for resources.
Contrary to H1, the growth of 93% of species
correlated with at least one soil nutrient, and many soil
nutrients had similar potential magnitudes of effect as
irradiance. Seedlings growing in very low light levels
might benefit from increased nutrient availability
through increasing light capture (Fahey et al. 1998).
Nitrogen is a key component of chlorophyll for light
capture and Rubisco for initial CO2 fixation (Evans
1989); thus higher N acquisition by seedlings could lead
to increased carbon gain even under light-limited
conditions (Walters and Reich 1997). Base cations also
were correlated with seedling growth; Mgþ is the central
atom in the chlorophyll molecule (Shabala and Hariadi
2005), and even under low-light conditions (,1% PAR),
seedling growth increased in response to Mgþ additions
(Burslem et al. 1995). Therefore, irradiance and soil
nutrients may be simultaneously limiting to seedling
growth in the forest understory, and increased Mgþ and
N may assist growth through improved light capture.
It was surprising that growth correlations with light
were not stronger and more prevalent as numerous
studies have shown the importance of increased light
availability to seedling growth (Augspurger 1984,
Poorter 1999). The unexpectedly weak growth–irradiance correlations could have arisen from the limited
range of existing light conditions, but which nevertheless
were representative of variation across 1 km of forest
understory over nine years. In contrast to other studies
(e.g., Kobe 1999), we did not intentionally stratify
variation in irradiance, but wanted to represent typical
conditions experienced by seedlings. We offer the caveat
that infrequent light measurements early in the study
could have partly obscured growth–light relationships
and thus underestimated irradiance effects. However,
strong correlations of irradiance through time suggest
that low frequency of light measurements early in study
was not a strong influence.
Contrary to H2, base cations (SBC) had greater
prevalence and magnitudes of effect than P, which is
consistent with accumulating empirical evidence (see
Lawrence 2003). Since base cations are more mobile
than P, they can be depleted more rapidly, especially in
tropical ecosystems where high precipitation levels
increase nutrient leaching (Chadwick et al. 1999). Base
cation leaching can result in low pH levels, high
aluminum concentrations, and toxicity effects that could
potentially affect plant growth. Because they co-varied,
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ELLEN K. HOLSTE ET AL.
Ecology, Vol. 92, No. 9
FIG. 4. Representative models of height growth with respect to irradiance and soil nutrients.
we combined Caþ, Mgþ, and Kþ into SBC, which
precluded testing for effects of individual elements, yet
each nutrient could influence seedling growth differently. For example, Kþ is the most mobile, and thus, most
leachable base cation, and could be most limiting to
growth. John et al. (2007) found that Kþ had the
strongest effects on species’ distributions in two out of
three studied forests, while Caþ and Mgþ were most
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SEEDLING RESPONSES TO SOIL RESOURCES
TABLE 1. Resource effect comparisons between irradiance and
soil nutrients across 94 woody species at La Selva Biological
Station, Costa Rica.
Resource effects (%)
Comparison
Greater irradiance effect
Greater soil nutrient effect
Effects indistinguishable
SBC PO4 Total N NO3 NH4þ
35
35
30
39
28
33
45
5
50
54
8
38
55
5
40
Notes: The table reports resource effect comparisons between
irradiance and soil nutrients among species for which irradiance
and at least one soil resource significantly influenced growth.
Resource effects are considered significantly different when P 0.05 and there is 29% overlap in 95% confidence intervals.
SBC is the sum of base cations (potassium, magnesium, and
calcium).
important in the third. Base cation availability and
growth are correlated in seedlings of species colonized
by mycorrhizae (Denslow et al. 1987, Burslem et al.
1995), and in particular, Caþ amendments increase
arbuscular mycorrhizal (AM) colonization (St. Clair
and Lynch 2005, Juice et al. 2006), the common
mycorrhizae associated with tropical forest plants.
Calcium effects mediated through AM fungi could
influence seedling growth through P uptake and defense
against pathogens and herbivores. However, mutualisms
with AM fungi also may be a substantial carbon sink
and could limit seedling growth (Johnson et al. 1997).
Other potential influences of base cations on seedling
growth could manifest through Mgþ’s role as a
structural component of chlorophyll, Caþ as a constituent of woody tissue (Baribault et al. 2010) and as a
correlate of photosynthetic rates (St. Clair and Lynch
2005), and the roles of Kþ and Caþ in signal
transduction and nutrient uptake (Stevens et al. 1993).
Although we are unable to untangle the effects of each
specific base cation in this study, base cations are
important in many chemical and physiological processes
that could influence seedling growth.
Even though N is generally more abundant than P in
tropical forests (Hedin et al. 2009), growth of over 50%
of species were correlated with some N form (consistent
with fertilization experiments [Lewis and Tanner 2000])
and less than one-third with PO4. Nitrogen could be
used to produce extracellular phosphatases, which are
8–32% N, and would alleviate P limitation through
hydrolyzing ester–PO4 bonds in soil organic P, and
releasing PO4 into soil solution for root uptake (Pant
and Warman 2000). Supporting this interpretation, N
fertilization increased phosphatase activity in a Hawaiian rain forest (Treseder and Vitousek 2001), while
increased P availability reduced extracellular acid
phosphatase activity (McLachlan 1980).
Seedling growth responses to PO4 may have been
underestimated because instantaneous pools of available
P (PO4 ) might have been too variable to provide an
integrated estimate of long-term availability, especially
since PO4 would be quickly assimilated when limiting
1835
(Vandecar et al. 2009). Our measure of total extractable
P contains both PO4 and some organic P (see Appendix
A) and thus incorporates some longer term pools, but
substituting total extractable P for PO4 in growth
models did not yield stronger P–growth correlations.
Nevertheless, more fully accounting for P cycling could
reveal a stronger influence of P.
Consistent with H3, irradiance and soil nutrients had
greater positive effects on the growth of light-demanding
species. In addition, the growth of six shade-tolerant
species was negatively correlated to irradiance. Shadetolerant species may experience photo-inhibition and
poor growth in sunflecks lasting 10 minutes or longer (Le
Gouallec et al. 1990, Krause et al. 2007), which can
contribute 10–85% of daily light levels (Pearcy 2007). The
inverse relationship between low-light survival and
magnitude of growth responses to nutrients conflicts with
other studies (Denslow et al. 1987, Lawrence 2001) that
examined only P and inorganic N. Our results suggest
that shade-tolerant species have a lower nutrient demand.
Lower resource demand among shade-tolerant species
may be a result of (1) greater seed nutrient reserves and/
or (2) slower growth rates. In this study, growth
responsiveness to resources was not correlated with
initial seedling height, a good surrogate for seed mass. In
addition, the relationship between initial seedling height
and low-light survival was significant, but moderately
weak (r ¼ 0.44; also see Wright et al. 2010). Thus, it is
unlikely that the negative correlation between low-light
survival and resource responsiveness arose from shadetolerant species having larger seeds that provide nutrient
carryover, which is consistent with the relatively short
time span of seedling dependency on reserves (Kitajima
2002). However, the shade-tolerant species in this study
tended to grow more slowly, and thus, would have lower
demand for nutrient incorporation into new tissue;
seedling growth calculated from maximum observed
resource levels was negatively (albeit weakly) correlated
with low-light survival (F1,88 ¼ 6.20, P ¼ 0.01, r ¼0.26).
We could not calculate potential or high-resource
TABLE 2. Comparisons of the magnitude of resource effects
between resources among species that responded to more
than one soil resource.
Resource effects (%)
Comparison
Greater SBC effect
Lesser SBC effect
Greater PO4 effect
Lesser PO4 effect
Greater total N effect
Lesser total N effect
Greater NO3 effect
Lesser NO3 effect
SBC PO4 Total N NO3 NH4þ
47
0
42
25
18
27
47
18
21
43
33
27
59
12
39
11
8
33
33
7
Notes: Resource effects denote the percentage of species in
which a given soil resource in the first column had a greater or
lesser effect on growth than other soil resources (columns 2–6).
Resource effects are considered significantly different (P 0.05) when there is 29% overlap in 95% confidence intervals.
1836
ELLEN K. HOLSTE ET AL.
Ecology, Vol. 92, No. 9
FIG. 5. Species-specific shade tolerance (mortality at 1% full sun) vs. growth responsiveness to resources (expressed as height
growth at maximum resource level [mm/month] per unit initial seedling height [mm1]). Statistics for individual resources: (A)
irradiance, F1,48 ¼ 12.30, P ¼ 0.001, r ¼ 0.45; (B) SBC, F1,35 ¼ 18.79, P ¼ 0.0001, r ¼ 0.59; (C) NO3, F1,28 ¼ 5.13, P ¼ 0.03, r ¼ 0.39;
(D) NH4þ, F1,31 ¼ 4.84, P ¼ 0.04, r ¼ 0.37; (E) PO4, F1,27 ¼ 3.42, P ¼ 0.08, r ¼ 0.34; and (F ) total N, F1,44 ¼ 0.17, P ¼ 0.07, r ¼ 0.68.
growth because of the generally low irradiance levels
encountered in the study; nevertheless, our results are
consistent with a broader trade-off between lowresource survival and high-resource growth (Kobe et
al.1995, Kobe 1999, Russo et al. 2008).
Conclusions
Predicting seedling growth under field conditions is
important to understanding forest dynamics and regeneration. Although irradiance has been regarded as the
primary determinant of seedling growth in wet tropical
forests, growth correlations with soil nutrients were
equally as important. Even though we cannot directly
evaluate if the different species’ responses to irradiance
and soil nutrients contributes to niche diversification
and diversity maintenance in wet tropical forests, our
study does demonstrate tremendous variation among
species in which resources influenced growth and the
magnitude and direction of those resource effects. This
interspecific variation satisfies important prerequisites
for niche partitioning along gradients of resources
(Kobe 1999). Moreover, the positive correlation among
species’ growth responsiveness to resources and survival
at low light is consistent with a general species’ trade-off
between low-resource survival vs. high-resource growth.
Both irradiance and soil nutrients were correlated with
September 2011
SEEDLING RESPONSES TO SOIL RESOURCES
seedling growth in the light-limited forest understory,
and therefore must be examined simultaneously across a
broad array of species with different life-history traits in
order to begin to understand potential mechanisms of
species coexistence and diversity in wet tropical forests.
ACKNOWLEDGMENTS
Financial support for this research was provided by NSF
(DEB 0075472, 0640904, 0743609) and the MSU Intramural
Research Grant Program. This research would not have been
possible without the hard work of Ademar Hurtado and Martin
Cascante for maintenance of field plots and data collection. We
appreciate the support of the OTS and La Selva Biological
Station staff, and we thank David Rothstein for methodological advice and use of equipment and facilities. The manuscript
benefited from critiques by Benedicte Bachelot, Tom Baribault,
Andrea Maguire, David Minor, Danae Rozendaal, Todd
Robinson, and two anonymous reviewers.
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APPENDIX A
Detailed methods for resource measurements (Ecological Archives E092-153-A1).
APPENDIX B
Spatial dependence of seedlings with residual growth variance per species and transect (Ecological Archives E092-153-A2).
APPENDIX C
Resource parameters of seedling growth rate, by species (Ecological Archives E092-153-A3).
APPENDIX D
Maximum magnitude of resource effects on the final height of seedling growth, by species (Ecological Archives E092-153-A4).
APPENDIX E
Correlations between species’ magnitude of responses and initial seedling size (Ecological Archives E092-153-A5).