Journal of Ecology 2012, 100, 969–979
doi: 10.1111/j.1365-2745.2012.01972.x
Does habitat specialization by seedlings contribute to
the high diversity of a lowland rain forest?
Margaret R. Metz*
Department of Integrative Biology, University of California, Berkeley, CA 94720, USA
Summary
1. One of the earliest hypotheses to explain high tropical forest diversity proposes that species are
differentially specialized in their germination or growth and survival to particular habitats.
2. I examined evidence for habitat associations in seedling density and demography in 9 years of
seedling dynamics data from Yasunı́ National Park, Ecuador, a lowland rain forest where previous
studies have demonstrated habitat preferences among adult trees. I included 136 species or morphospecies from multiple annual seedling cohorts with known age of recruitment.
3. Approximately 90% of the species examined demonstrated negative or positive associations with
one or more topographic habitats in their recruitment, growth and ⁄ or mortality at some point in
the study, and approximately 60% of species had significant associations in at least half of the census periods studied. The survival of newly recruited seedlings varied among seedlings in response to
topographic gradients, indicating the potential for species to partition habitat niches at a young
stage.
4. There was significant inter-annual variation in seedling habitat associations, indicating the characteristics of the topographic niche important to seedling performance change through time. This
variability alone can contribute to the maintenance of species diversity through storage effects.
While associations may also be weak or ephemeral, the seedling dynamics for many species
supported the possibility that associations seen in adult populations develop through differential
mortality across habitats as seedlings.
5. Synthesis. That species’ seedlings perform differently among topographic habitats and that these
differences are detectable very early on in a plant’s life indicate the potential for the abiotic environment to mediate or exaggerate the roles of other mechanisms in influencing the composition of the
understorey seedling assemblage.
Key-words: determinants of plant community diversity and structure, environmental heterogeneity, niche differentiation, plant population and community dynamics, regeneration niche,
spatial autocorrelation, torus translation, Yasunı́ National Park
Introduction
Ecologists have long generated hypotheses to explain the maintenance of the high levels of species diversity observed in tropical forests (e.g. Aubréville 1938; Janzen 1970; Connell 1971,
1978; Orians 1982; Hubbell & Foster 1986; Hurtt & Pacala
1995; and see review in Wright 2002). Proponents of a ‘nicheassembly’ view emphasize the dependence of community
composition on differential specialization to particular environmental characteristics. Variants of this hypothesis posit
that tree species are differentially specialized in their requirements for germination, or in their later growth and survival, to
specific edaphic conditions (e.g. Richards 1952; Janzen 1974;
*Correspondence author. E-mail: [email protected]
Whitmore 1984; Clark, Clark & Read 1998), topographic habitats (Svenning 1999; Harms et al. 2001; Valencia et al. 2004)
or light availability (Ricklefs 1977; Orians 1982; Svenning
2000). Species differ in the environmental conditions they
require for successful establishment and early survival (Grubb
1977), and the availability of these conditions at any site may
vary in time so that suitable germination sites can be ephemeral
or vary with biotic interactions (Fine, Mesones & Coley 2004;
Metz, Sousa & Valencia 2010). Critics of the ‘niche-assembly’
hypothesis have argued that environmental heterogeneity and
habitat specialization are not sufficient to explain the high
levels of species richness observed in tropical communities
(Connell 1978; Hubbell & Foster 1986) where over 300 tree
species can coexist in a single hectare (Valencia, Balslev & Paz
y Miño 1994). Not only do all plant species require the same,
2012 The Author. Journal of Ecology 2012 British Ecological Society
970 M. R. Metz
relatively small number of resources, they obtain resources via
almost identical mechanisms.
Nevertheless, a number of authors have revitalized arguments in favour of the importance of niche specialization
(Silvertown 2004; John et al. 2007) or community assembly via
environmental filtering of species with traits favourable to
survival in a particular habitat (Kraft, Valencia & Ackerly
2008; Kraft & Ackerly 2010). There have been several recent
examples with strong evidence of habitat associations in tropical tree species across topographic gradients (Webb & Peart
2000; Harms et al. 2001; Valencia et al. 2004; Gunatilleke
et al. 2006; Queenborough et al. 2007), degrees of topographic heterogeneity (Potts et al. 2004), soil types (Cannon &
Leighton 2004), or gradients of soil minerals and nutrients
(John et al. 2007) in large-scale plots covering between 4.5 and
52 hectares of tropical forest. These associations were typically
assessed using static measures (e.g. relative species abundance
at one time) and were common among species, but were only
examined in adults and saplings, generally > 1 cm DBH.
Although habitat associations were widespread among species
in these studies, the authors also concluded that habitat associations were not sufficient to represent the primary mechanism
maintaining high levels of diversity in tropical forests. Many
species were generalists or showed neutral associations with
habitats (but see Gunatilleke et al. 2006), and species with
significant associations also demonstrated significant distributional overlap with other species.
If species disperse everywhere yet exhibit distinct patterns of
habitat association (i.e. niches), plant species must have differential success across environmental gradients in seedling establishment, growth and survival that leads to changes in
abundance in different habitats. Such an effect may be difficult
to detect in the field, as species do not have universal dispersal
to reach all sites, site characteristics may vary through time,
and the majority of seedlings tend to occur near the parent,
likely within a similar habitat (Nathan & Muller-Landau
2000). Thus, the spatial patterns of species’ seedling abundance caused by limited dispersal can be difficult to differentiate from spatial patterns caused by differential performance in
response to environmental variation. In addition, the environmental characteristics that adults or saplings respond to may
occur at quite different scales from those relevant to seedlings
because of the strong asymmetric competition for resources
imposed on seedlings by their larger neighbours (Wright
2002). The survival or growth of small seedlings may be more
influenced by microtopography or the local light environment
over small areas (square centimetres or metres) than by features measured at the scales relevant to adults (perhaps tens of
square metres). Nevertheless, for the patterns to be evident in
adult assemblages, there must be some relationship between
the characteristics shown to correlate to adult associations and
to seedling performance through time, despite the mismatch in
scales.
Few studies have considered habitat specialization during
early life stages. Webb & Peart (2000) examined habitat associations in seedlings ‡ 5 cm tall using relative abundance indices.
In comparison with habitat associations demonstrated by
saplings and adults, they found that fewer species demonstrated associations as seedlings. Comita, Condit & Hubbell
(2007) examined distributions of established seedlings, ‡ 20 cm
tall, and compared their habitat associations to patterns found
in trees ‡ 1 cm DBH in Panama, where the prevalence of habitat associations had already been established (Harms et al.
2001). Using relative abundance as a measure of habitat preference, only one-third of the species that showed associations as
adults also demonstrated them as seedlings. The results from
both studies are consistent with a scenario where adult habitat
associations develop over years of differential growth and
survival across habitats. In such a case, the static patterns of
abundance in younger stages may not reflect species’ habitat
associations, while tracking individuals through time across
habitats would reveal differential survival that eventually
causes the association patterns seen in older life stages. Indeed,
patterns of seedling mortality tracked across wet and dry seasons in Panama suggest that associations may develop because
of differences in water availability across habitats and drought
sensitivity across species (Comita & Engelbrecht 2009).
Here, I present an analysis of 9 years of seedling dynamics
data from a 50-hectare forest dynamics plot in Yasunı́
National Park, Ecuador, that examines the evidence for habitat specialization at the seedling stage by tracking changes in
seedling abundance and performance across habitats and
through time. I examined recruitment, growth and survival of
over 18 000 seedlings of known age from 136 woody species to
ask: (i) Do seedlings at Yasunı́ demonstrate significant associations with topographic habitats or performance biases across
habitats in growth or survival? (ii) Do species vary in their
response to topography to indicate niche partitioning among
species? The long-term and community-level data set permits
an examination of these questions across eight annual seedling
cohorts from the time of seedling establishment through survival and growth over multiple years for many species of trees,
shrubs and lianas.
Yasunı́ is an ideal site to examine the role of habitat associations in maintaining forest diversity because it is extremely
species-rich and because there is ample evidence at older life
stages that tree species display differential abundances across
habitats: the composition of saplings and adults has been
shown to vary among topographic habitats (Valencia et al.
2004; Queenborough et al. 2007), and 40% of species’ distributions are significantly correlated with the distribution of soil
nutrients (John et al. 2007). Valencia et al. (2004) determined
that approximately one-quarter of Yasunı́’s > 1100 tree species were habitat specialists as adults or saplings, one-quarter
were generalists, and the remainder differed in abundance
among habitats, but without strong enough patterns to permit
categorization of habitat preferences. Evidence from the functional traits of species and phylogenetic relationships among
tree species at Yasunı́ also suggests a strong role for environmental filtering of species assemblages (Kraft, Valencia &
Ackerly 2008; Kraft & Ackerly 2010). Here, I investigate
whether patterns exhibited by adults develop from early
patterns of differential growth and survival across habitats by
seedlings.
2012 The Author. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100, 969–979
Seedling habitat associations and tropical diversity 971
Materials and methods
STUDY SITE
This research was conducted inside the Yasunı́ Forest Dynamics Plot
(FDP), a 50-ha plot that is part of a network of large-scale, long-term
forest dynamics plots coordinated by the Center for Tropical Forest
Science (CTFS) at the Smithsonian Tropical Research Institute
(STRI). The Yasunı́ FDP is located in the northern part of Yasunı́
National Park in eastern Ecuador (041¢ S, 7624¢ W). Within the
plot, all stems ‡ 1 cm DBH have been mapped, identified and measured for girth and have been censused every 5 years, starting in 1995.
Yasunı́’s evergreen lowland wet forest lies within the upper Amazon
basin, one of the most species-rich regions in the world (Gentry 1992).
There are approximately 1100 tree species in the 50-ha Yasunı́ FDP
(Valencia et al. 2004), and levels of up to 300 tree species per hectare
have been observed in the area (Valencia, Balslev & Paz y Miño 1994).
Yasunı́ has an aseasonal climate, receiving a mean annual rainfall of
3081 mm, with constant temperature throughout the year (Losos &
Leigh 2004). The plot lies at 230 m above sea level, and there is a
33.5 m difference between the plot’s highest and lowest points. Losos
& Leigh (2004) describe the site and the Yasunı́ FDP in greater detail.
combining ridge-top (elevation ‡ 227.2 m, slope < 12.8 and convexity > 0) and high-slope (elevation ‡ 227.2 m, slope ‡ 12.8 and
convexity > 0); (ii) slope, combining high gully (elevation ‡ 227.2 m,
slope ‡ 12.8 and convexity < 0) and low-slope (elevation
< 227.2 m and slope ‡ 12.8); and (iii) valley (elevation < 227.2 m
and slope < 12.8). While their topographic categorizations result in
few habitat types, the topography in Yasunı́ and other forests is significantly correlated with a number of soil nutrients and resources
that affect plant distributions (John et al. 2007), so that these simple
topographical categories may stand as proxies for many different
environmental niches. In addition to the topographical categories,
there is a former oil company helicopter landing circle in the northwestern portion of the plot, dominated by the pioneer Cecropia sciadophylla, which is classified as secondary forest. None of the seedling
census stations was located in this area, and quadrats with that classification were not used in these analyses.
Seedling census stations were categorized according to the habitat
category of the 20 · 20 m quadrat in which they were located. With
these classification criteria, approximately 40%, 25% and 33% of the
quadrats in the Yasunı́ FDP are assigned to the valley, mid-slope and
upper ridge habitats, respectively (Fig. S1). The distribution of the
seedling census stations samples these habitats in representative proportions (v2 = 12, d.f. = 9, P = 0.2133).
SEEDLING CENSUS DESIGN
In 2002, I established 600, 1-m2 seedling census plots within the
Yasunı́ FDP (Metz, Sousa & Valencia 2010) in association with a network of 200 seed traps that had been previously established as part of
other ongoing phenological studies at Yasunı́ (Persson 2006).
Together, a seed trap and its adjacent seedling plots comprise a seedling census station. The stations are arrayed systematically every
13.5 m along the trails, on alternating sides of the trail and at random
distances of 4–10 m into the forest from the trails (See Fig. S1a).
In annual June–July censuses of the plots from 2002 to 2010,
I mapped, identified and marked every seedling recruited into the plots
and measured the height of all marked individuals. The 2002 baseline
census included all individuals < 1 cm DBH that were already established in the plots and thus are of an unknown age. I restricted the
following analyses, however, to include only seedlings that were
recruited into the study plots over the eight census intervals following
the 2002 baseline census and thus are of known age. I refer to these
hereafter as ‘seedlings’, although species may differ greatly in stature
or the length of time cotyledons are retained. ‘Recruits’ are seedlings
that enter the annual seedling census for the first time in particular
year. Data from the annual censuses permit estimation of speciesspecific and age-specific rates of recruitment, growth and survival.
FOCAL SPECIES
I restricted the analyses presented here to seedlings of known age, or
only those seedlings that recruited after the baseline census in 2002,
grouped into eight annual cohorts. Only a portion of the > 600 species or morphospecies identified as seedling recruits in this study have
sample sizes large enough to allow rigorous statistical analyses. I
restricted the analyses to the 136 species or morphospecies that
recruited new seedlings into at least 10 different census stations over
the course of the study. These included trees, shrubs and lianas from
94 genera and 44 families (Table S1). The most species-rich group
was the legumes (Fabaceae), with 24 species included in the analyses,
12 of which were in the genus Inga. The palms (Arecaceae) were also
abundant with eight species, including one of the most abundant trees
in the Yasunı́ FDP, Iriartea deltoidea. Spatial and temporal heterogeneity in recruitment was largely responsible for limiting the number
of species that met our sample size criterion.
The tests described later focus on two separate age classes of seedlings. The torus permutation tests examine general seedling patterns
by including both young-of-the-year seedling recruits and older seedlings £ 50 cm height that have survived one or more years following
recruitment. The generalized linear mixed effects survival model
focuses only on newly recruited seedlings to standardize comparisons
among seedlings of the same age.
HABITAT DESIGNATIONS
Each 20 · 20 m quadrat in the Yasunı́ FDP has been assigned a
mean elevation (m), slope from the horizontal (degrees) and an index
of convexity (see detailed descriptions in Harms et al. 2001 and
Valencia et al. 2004). Valencia et al. (2004) used these to assign habitat categories to the western 25 ha of the Yasuni FDP, and I extended
these categories to the eastern 25 ha of the study area, as the network
of seedling census stations traverses the entire 50-ha area. Valencia
et al. (2004) initially examined five topographic habitats, but condensed these to three categories when the species composition in two
pairs of habitats showed as much within-habitat similarity as
between-habitat similarity, making the pairs indistinguishable.
Following the conventions of their study, I assigned each 20 · 20 m
quadrat to one of the three condensed topographic habitats: (i) ridge,
TESTS OF HABITAT ASSOCIATIONS USING TORUS
PERMUTATIONS
I conducted torus permutational tests of habitat associations or performance bias separately for each species in each census year or interval. Not all species were abundant in every census, so analyses were
restricted to species that had seedlings occurring in at least five census
stations during the focal census (for analyses of abundance) or at the
start of the census interval (for analyses of growth or survival).
Although mortality for newly recruited seedlings is higher than for
established seedlings, some individuals survive to the next census
interval, and the number of stations at which they occur can increase
through recruitment. In addition, the 2005 census had far higher
2012 The Author. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100, 969–979
972 M. R. Metz
recruitment than was observed in other years (Metz et al. 2008), and
the number of species meeting the sample size requirements also
increased. Thus, the number of species analysed tended to increase
each year.
For each species that fit the minimum sample size requirements in
each census, I calculated the abundance, growth rate and survival
rates at each census station and averaged station-level measures
across stations within a habitat. There were two measures of abundance: seedling density (m)2) and relative abundance, or the number
of the focal species’ seedlings divided by the total number of seedlings
at the station. To assess whether a species’ performance varied among
habitats, potentially accounting for its differential distribution, I used
three measures of seedling success, standardized to annual rates:
absolute growth in height (cm; measured as height of apical meristem
from soil surface), relative growth (the difference in the logarithm of
the height measurements) and survival (measured as the proportion
of seedlings present at a station in one census that survive to the following census). Annual growth rates were averaged across all seedlings of the focal species to obtain a station-level average.
Apparent differences in seedling abundance among habitats may
be a simple coincidence of the spatial structure of the topography and
spatial patterns of seedling distribution and not a result of species’
preferences because both the topography and the distribution patterns of seedlings are spatially autocorrelated. The initial distributions of seedlings may continue to influence seedling growth or
survival if, for example, related individuals are dispersed near each
other and perform more similarly than seedlings from other parents.
I used torus translations of the topography, as described in Harms
et al. (2001), to decouple the spatial coincidence of the topography
and overlying seedling distributions, while preserving the spatial
structure of each. In this method, the habitat map was shifted in 20-m
steps to the north or east while retaining the same spatial structure of
the true topography. As the habitat map ‘fell off’ the end of the FDP
boundaries, the boundary wrapped around and connected to the
other side, as in a torus (Fig. S1b). Each of the 1250 possible translations of the map was also mirrored and ⁄ or inverted (Fig. S1c, d, e),
leading to 5000 permutations of the map, one of which was the true
habitat map. The seedling census network was overlaid on each map,
and measures of seedling abundance or performance in each habitat
calculated on every translated map created a null distribution that I
compared to the values observed on the original ‘true’ map. If the
observed values were in the extremes of the null distribution, the species was considered to have a significant association with that habitat.
Examining habitat associations in this way is a two-tailed test of
‘local’ significance (sensu Cannon & Leighton 2004) that determines
whether seedling density, growth or survival in a habitat on the true
map was more extreme than 97.5% of the seedling performance values measured in that habitat on all 5000 maps. A significant positive
or negative habitat association or performance bias indicated that
a species was significantly more ⁄ less abundant or grew significantly
faster ⁄ slower or survived significantly better ⁄ worse in a habitat than
would be expected from a chance spatial alignment of the seedling
distributions with the topography of the plot.
PARTITIONING TOPOGRAPHIC NICHE AXES
I used a generalized linear mixed effects model (GLMM) to examine
the relationship between topography in the Yasunı́ FDP and the survival of newly recruited seedlings, and to understand the potential for
species to partition topographic niche axes as seedlings. The analysis
included all recruit cohorts of seedlings from the 136 focal species.
There are seven cohorts of known-age seedlings in the data set,
recruiting in the 2003–09 censuses, for which performance can be
tracked until 2010. Here, I present the results of 3-year survival for the
five cohorts that have been in the study for this period. Similar models
for 1-year performance (seven cohorts) or 5-year performance (three
cohorts) had qualitatively similar results and are not presented here.
Survival was modelled using the logit transformation of the survival
probability for individual seedlings and a binomial error structure.
The independent predictor variables were continuous topographic
variables (mean elevation, slope and convexity, as described above)
for the 20 · 20 m quadrat in which the focal seedling’s census plot
was located, and the initial height (cm) of the newly recruited seedling,
from the soil surface to the apical meristem. Each of these variables
was centred by subtracting the mean prior to analysis. I included species identity in the model as a random factor and allowed species to
vary in their response to each topographic variable (the slope or intercept of the relationship between survival and, for example, mean elevation). This allowed species to have positive or negative relationships
with topography (indicated by direction and strength of the parameter
estimate) or to vary in their baseline mortality rates (the intercept of
the relationship). Large variation among species would indicate
partitioning of topographic niches. To account for the spatial nonindependence of seedlings located within the same plot, and within
plots at the same census station, I included the random effect of plot
nested within station. To account for differences in overall survival
across cohorts due to annual variation in climate or other factors,
I also included the cohort identity for each recruit. This was included
as a fixed factor in the model because the low number of replicate
cohorts precluded decent estimation of this effect as a random factor.
I confirmed that the model structure including plot and census station location accounted for any potential spatial autocorrelation not
related to topography (e.g. common light environments or biotic factors at a plot) by examining correlograms of the model’s Pearson
residuals and a Moran’s I test for spatial autocorrelation. No residual
spatial autocorrelation was detected.
All the analyses were conducted in the statistical programming language R, version 2.14.10 (R Development Core Team 2011). The survival model was conducted using the lme4 package (Bates & Maechle
2010), and residual spatial autocorrelation was checked using the ncf
package (Bjornstad 2009) and the methods of Dormann et al. (2007).
Results
ASSEMBLAGE-WIDE PERFORMANCE
Measures of abundance, growth and survival varied among
habitats and years for all species combined (Fig. 1). The patterns were similar whether examining seedlings of all known
ages combined or only the young-of-the-year recruits
(Fig. S2), although the latter examination included fewer species. On average, the density of each species was lower than
one individual per m2 and ranged from 0.5 ± 0.07 m)2
(mean ± SE) in ridge stations in 2003 to 1.5 ± 0.7 m)2 in
valley stations in 2005. In 2003–05, the mean density of a
species was highest in the valleys but in other years was higher
in the slope or ridge habitats (Fig. 1a). As more seedlings
recruited into the study, the mean relative abundance of any
one species decreased, especially in the 2005 census which had
higher recruitment overall (Metz et al. 2008).
Overall growth rates were quite variable among intervals,
and the ranking among habitats changed often for both
2012 The Author. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100, 969–979
Seedling habitat associations and tropical diversity 973
(a) Abundance
1.5
0.20
Proportion
Seedlings per m2
0.25
Valley
Slope
Ridge
2.0
1.0
0.5
0.10
0.05
77
0.0
0.15
106
129
131
134
136
134
130
0.00
2003 2004 2005 2006 2007 2008 2009 2010
2003 2004 2005 2006 2007 2008 2009 2010
(b) Growth rates
0.30
4
0.25
log(cm)/year
cm/year
3
2
0.20
0.15
0.10
1
0.05
74
0
95
120
123
132
130
128
2003 2004 2005 2006 2007 2008 2009 2010
0.00
2003 2004 2005 2006 2007 2008 2009 2010
(c) Survival rate
Proportion surviving/year
0.8
0.6
0.4
0.2
77
0.0
106
129
131
134
136
134
2003 2004 2005 2006 2007 2008 2009 2010
Fig. 1. Overall seedling performance. The abundance, growth and survival of seedlings in valley, slope and ridge habitats vary through time and
among habitats. At each station, performance was averaged across species, weighted equally, before being averaged across stations within a habitat. Error bars are the standard error of station values within a habitat. Grey numbers at the base of the graph indicate the number of species
included in the average. Abundance (a): mean species seedling density (left panel) and mean species relative abundance (right panel). Growth
rates (b): species mean annual absolute growth rate (left panel) and species mean annual relative growth rate in (right panel). Survival rates (c):
mean species proportion surviving each year. See Fig. S2 for similar results of young-of-the-year recruits only.
absolute and relative growth rates (Fig. 1b). Absolute growth
rates ranged from 0.8 ± 0.5 cm y)1 in ridge stations over
2003–04 to 3.0 ± 1.1 cm y)1 (mean ± SE) in slope stations
over the 2005–06 interval.
Annual survival rates ranged from 56.8% ± 2.5
(mean ± SE) in valley stations over the 2007–08 interval
to 76.7% ± 3.4 in ridge stations over the 2003–04 interval. In
general, the rates differed little among habitats or years,
although survival tended to be lower in the valley overall
(Fig. 1c).
TESTS OF HABITAT ASSOCIATIONS USING TORUS
PERMUTATIONS
The vast majority of species analysed did show significant habitat associations (Table 1). At least one-third and up to three
2012 The Author. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100, 969–979
974 M. R. Metz
quarters of the species had a significant positive or negative
association measured by their relative or absolute abundance
with at least one habitat type in any given year (Table 1), and
many species had similar associations over multiple years
(Table S2). There were more significant associations measured
by density than by relative abundance in every year. Far fewer
species, 5.6–22.7%, had differential success among habitats
measured by their absolute or relative growth rates over each
census interval (Table 1), but when success was measured by
rates of survival, approximately half of the species had a significant association with at least one habitat (Table 1). Generally, species associations were not evident in each census they
were tested, and, although most associations were consistent
within a habitat, there were some species that switched
between positive and negative associations in different years
(Table S2). As the duration of the study increased, and more
annual seedling cohorts could be included, there were more
Table 1. Percentage of species demonstrating significant habitat
associations in torus permutation tests. The number of species tested
in each census or over each interval and the percentages of those
species that showed a significant positive or negative association with
at least one habitat type as measured by a) relative abundance of the
species in a habitat (%) or density (seedlings per m2); b) relative
growth rates (log(cm) year)1) or absolute growth rates (cm year)1);
and c) survival rates (proportion surviving year)1). Species may have
an association with more than one habitat type. See Table S2 for
detailed summary of species’ responses
Census
Species No.
Relative, %
Density, %
(a) Abundance
2003
21
2004
48
2005
84
2006
92
2007
94
2008
108
2009
107
2010
110
52.4
50.0
39.3
52.2
45.7
46.3
42.1
41.8
76.2
72.9
65.5
73.9
69.1
68.5
68.2
72.7
Interval
Relative, %
Absolute, %
(b) Growth rates
2003–04
18
2004–05
34
2005–06
62
2006–07
61
2007–08
66
2008–09
87
2009–10
87
5.6
14.7
12.9
16.4
22.7
16.1
16.1
0.0
17.6
14.5
13.1
22.7
18.4
16.1
Interval
Survival, %
Species No.
Species No.
(c) Survival rates
2003–04
21
2004–05
48
2005–06
84
2006–07
92
2007–08
94
2008–09
108
2009–10
107
47.6
47.9
52.4
43.5
44.7
51.9
46.7
species with sufficient sample sizes for analysis and more species that showed at least one significant association (Fig. 2).
The proportion of the total species demonstrating at least one
significant positive or negative association levelled off at
approximately 90% (for measures of density or survival) once
five or more annual cohorts were included (Fig. 2); 60% of
species had significant associations in four or more of the
tested census periods.
PARTITIONING TOPOGRAPHIC NICHE AXES
Topographic descriptors (measured by slope, convexity and
elevation) were not significant predictors of overall recruit survival because there was great variation among individual species in their response to the topography (Table 2, Fig. 3). The
large variation among species in the intercept of the survival
relationship indicated differences in the baseline mortality rate,
and the variation among species in the slope parameter estimates (both the direction and strength) for the relationship
with topography demonstrated the potential for partitioning
of these niche axes. In particular, the response to the topographic slope was quite variable (Table 2, Fig. 3). Many species’ survival appeared insensitive to changes in the
topographic slope, while others survived better or worse as
slopes steepened. Species that had a particularly sensitive
response to slope and tended to survive better on steeper slopes
also tended to be found across a wider range of slopes (including the steepest) than were species that survived better in flatter
areas and tended to be found over a more narrow range of
slopes. There was also significant variation among cohorts in
overall survival, indicating the importance of inter-annual variation in the response to topography.
EXAMPLES OF SPECIES’ PATTERNS
Both sets of analyses demonstrated significant variation
among species and years in the relationship between seedling
dynamics and topography. Some species demonstrated qualitatively similar patterns in abundance and performance year to
year, while other species were much more variable (Table S2).
For example, Cedrelinga cateniformis tended to have a negative
association with or performance biases in the valley and a positive association with slope. Other species, like Pourouma minor,
Matisia malacocalyx or Talisia novogranatensis, had positive
associations in some years and negative associations in other
years in the same habitat type. Associations detected by
patterns of abundance often matched performance biases
detected in growth or survival rates (e.g. Brownea grandiceps in
the valley, or Pouroma tomentosa on slopes and ridges). In
contrast, survival rates in some species were higher than
expected by chance in habitats where the species also tended to
be more rare (i.e. a positive association measured by survival
rates, but a negative association measured by abundance), such
as Inga umbractica or Tapirira guianensis in the slope habitat.
The result for T. guianensis was confirmed in the GLMM analysis of survival of seedling recruits where this species survived
better with increasing slope, but was not found on the steepest
2012 The Author. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100, 969–979
Seedling habitat associations and tropical diversity 975
1.0
140
Density
Rel. Abundance
Abs. Growth
Rel. Growth
Survival
100
0.8
Proportion
No. species
120
80
60
40
0.4
0.2
20
0
0.6
2
4
6
0.0
8
2
No. cohorts studied
4
6
8
No. cohorts studied
Fig. 2. Prevalence of habitat associations with variation in study duration. As the length of the seedling study increases, more species fit the minimum sample size requirements (detailed in Methods) for inclusion in this study. As the number of annual seedling cohorts included in the study
increases, so too does the number of species found to have a significant association (negative or positive) with at least one habitat in at least 1 year
(left panel). The proportion of species studied that demonstrate at least one association (right panel) increases, but appears to level off after about
five cohorts have been studied. The number of species demonstrating associations is calculated separately for abundance, growth and survival.
Here, associations are determined from the torus permutational tests.
of slopes (Fig. 2). The results of all torus permutation tests are
available in Supplementary Table S2.
Discussion
DIFFERENCES IN PERFORMANCE ACROSS HABITATS
Groups
Random effects
Plot (Station)
Station
Species
Species
Species
Species
Parameter
Intercept
Intercept
Intercept
Slope
Convexity
Mean Elevation <
Estimate
Fixed effects
(Intercept)
Slope
Convexity
Mean Elevation
Height
Cohort (2004)
Cohort (2005)
Cohort (2006)
Cohort (2007)
Variance
)0.725
0.001
0.023
0.006
0.052
)0.754
)0.875
)0.930
)1.040
Model AIC 6045.2.
0.440
0.222
1.114
0.001
0.002
0.001
SE
0.664
0.471
1.055
0.037
0.047
0.009
Odds Ratio SE
0.484
1.001
1.023
1.006
1.054
0.470
0.417
0.394
0.354
0.159
0.012
0.051
0.013
0.007
0.155
0.134
0.144
0.150
The results from this multi-year study demonstrate that young
seedlings of most species show differential abundance and performance across topographic habitats. Abundance, growth
rates and survival rates for the seedling assemblage as a whole
varied across the ridge, slope and valley habitats, but these patterns often differed among years. Topography is significantly
1.0
0.8
Predicted survival
Table 2. Survival of newly recruited seedlings over 3 years. Results of
a generalized linear mixed effects model with binomial errors where
survival for 3 years following recruitment was predicted by initial
seedling height and the continuous topographic variables of slope,
convexity and mean elevation of the 20 · 20 m quadrats where
seedling plots were located. Random effects to account for spatial
non-independence included the seedling plot nested within the census
station and species identification. The slope and intercept of the
relationship between survival and topography were permitted to vary
among species. The recruit cohort was included as a fixed effect to
account for overall differences in survival across years. Seedling
height and the topographic variables were each centred prior to
analysis. See Fig. 3 for illustration of variation among species in
response to the slope of the area
0.6
pressc
tapigu
eschco
0.4
neeaco
ingaoe
eschg1
pse1l2
iriade
0.2
0.0
P-value
< 0.001
0.913
0.653
0.629
< 0.001
< 0.001
< 0.001
< 0.001
< 0.001
sim3co
0
5
10
15
20
25
30
Slope of 20 × 20 m plot
Fig. 3. Species partitioning topographic niches. The fitted relationships for seedling survival across variation in the topographic slope of
the 20 · 20 m quadrat in which seedlings are found. See Table 2 for
the results of the full model. Each line represents a species’ predicted
survival against variation in slope with all other predictor variables
held at their median variable. The length of the line indicates the
range of measured topographic slopes within which seedlings of this
species were censused. There is great variation among species in their
response to topography, and many species appear relatively insensitive to changes in slope. Some species are highlighted in red or blue
for being particularly responsive to topography, performing better on
steeper or less steep slopes, respectively.
2012 The Author. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100, 969–979
976 M. R. Metz
correlated with many soil nutrients at Yasunı́ and elsewhere
and also stands as a proxy for many soil characteristics that are
important resources for young plants, such as water availability and drainage, and soil bulk density (Silver et al. 1994; John
et al. 2007). The availability of different resources may interact
to create an environment that changes from year to year.
The majority of species showed non-random patterns of
associations with one or more habitat, such that abundances
or survival rates in one habitat were significantly higher or
lower relative to other habitats than would be expected by a
chance relationship between seedling performance and habitat
characteristics. In addition, early seedling survival varied significantly among species in response to variation in topographic variables, suggesting that species may partition
topographic niches. That these local habitat associations are
evident in the first few years of a tree’s existence, indeed even in
young-of-the-year recruits, indicates a strong potential for
environmental characteristics to play an important role as a filter for species distributions through increased survival in some
habitats and decreased survival in others. If individuals of
some species accumulate preferentially in certain habitats, the
bank of shade-tolerant seedlings in understorey, or the
‘advanced regeneration’, will differ among habitats. There is
generally high survival of understorey seedlings and saplings
existing at the time of gap formation, so that canopy turnover
through gap regeneration may strongly depend on advanced
regeneration rather than new recruitment into gaps (Uhl et al.
1988; Fraver, Brokaw & Smith 1998; Brokaw & Busing 2000).
Habitat effects that influence the composition of seedlings in
the understorey, such as the differential survival among habitats demonstrated here, could therefore play a role in determining the composition of the canopy, especially as the effects of
these processes accumulate over the many years required for
gap turnover.
TRACKING INDIVIDUALS ACROSS YEARS
I hypothesized that evidence of habitat associations would be
stronger in seedlings when measuring performance biases in
growth or survival because these rates would reflect the environmental filtering of species in habitats that are more or less
suitable to a species’ traits, while patterns of seedling abundance would reflect broader dispersal to many habitats. Contrary to my expectations, I found that strong habitat
associations were least prevalent when measured by growth
rates and found as frequently in survival rates as in the measures of abundance. Both survival rates and measure of abundance provided a strong signal of differential performance
across habitats for a large proportion of species. Once established, rain forest seedlings spend many years as advanced
regeneration in the understorey (Connell & Green 2000). They
may need to survive long enough to take advantage of several
cycles of canopy openings and closings before reaching the
overstorey (Grubb 1977; Delissio et al. 2002). These results
show that for many species, seedlings survive differently across
habitats and thus may have more opportunities to recruit into
the overstorey in some habitats than in others.
In contrast to survival rates, growth rates provided much
less evidence for habitat associations in seedlings. While differences in growth should also be important in creating patterns
of habitat associations, seedling growth is difficult to measure
without error, and seedling growth rates are notoriously variable, with much noise hindering the detection of any biological
signal (Baraloto & Goldberg 2004). Seedlings suffer mechanical damage from falling debris or passing animals that may be
random with respect to the topographic habitat. Further, herbivory and browsing alone are enough to make negative
growth rates very common in seedlings. Previous work at
Yasunı́ and other forests showed that assemblage-wide seedling growth rates fit a bi-exponential distribution because of
the symmetric distribution of negative and positive growth
rates and the long tails in each (Metz et al. 2008). Seedlings
were most often recruiting into and persisting in the very
shaded microsites of the forest understorey (and rarely into
light gaps), so growth may not be expected to provide a very
strong signal. The confounding influences of a shaded understorey and damage from biotic or other physical factors lead to
a noisy mixture of positive, negative and stagnant growth rates
that may swamp signals of any positive or negative effects of
the topographic environment on seedling growth.
COMPARISON OF SEEDLING AND ADULT PATTERNS OF
HABITAT ASSOCIATION
Given the habitat associations exhibited by adults at Yasunı́
(Valencia et al. 2004; John et al. 2007; Queenborough et al.
2007), I expected seedling performance to provide evidence for
the filtering effect of habitat through differential growth and
survival across habitats. Although Valencia et al. (2004) did
not directly assess species-specific habitat preferences, the habitat associations I found are similar to some of the patterns in
adult dominance and distributions at Yasunı́ in their study.
For example, Rinorea lindeniana, Yasunı́’s second most common tree ‡ 1 cm DBH, is the first and third most dominant
species in the ridge and slope habitats, respectively, but is less
abundant in the valley habitat (Valencia et al. 2004). Similarly,
R. lindeniana seedlings were significantly less abundant in the
valley habitat in most years, measured by density and ⁄ or relative abundance, and tended towards lower growth rates and
survival rates at valley census stations (Table S2). Two of the
most common species at Yasunı́, Iriartea deltoidea and Eschweilera coriacea, are dominant in all habitats (Valencia et al.
2004), and similarly, seedlings of these species did not generally
have differential performance among habitats. While the
patterns of seedling abundance and performance were suggestive of adult associations for many species, there were also
several species where seedling patterns did not immediately
appear to reflect adult patterns.
Queenborough et al. (2007) used torus translations to test
habitat associations for adults and saplings in the Myristicaceae family, and the seedling habitat associations for six of
those species were also studied here, permitting a direct comparison of patterns (Table S2). Iryanthera hostmannii adults
did not have significant associations with topographic
2012 The Author. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100, 969–979
Seedling habitat associations and tropical diversity 977
habitats, and accordingly, the seedlings tended to perform
equally among habitat. Otoba glycycarpa seedlings survived
significantly better in slope and valley habitats, but tended to
be less common in these habitats, although the adults had significant positive associations there (Queenborough et al.
2007). Virola elongata, V. ‘microfuzzy’ and V. pavonis had no
significant associations as adults (Queenborough et al. 2007)
and, as seedlings, varied between positive and negative associations in all habitats (Table S2). Virola duckei seedlings tended
to be significantly less abundant, but have significantly higher
survival rates, in slopes and valleys (Table S2) although the
adults were significantly negatively associated with valleys and
positively associated with slopes (Queenborough et al. 2007).
For these six Myristicaceae species, the patterns of differential
seedling abundance and performance among habitats
observed here support the hypothesis that adult associations
could develop from differential mortality at the earliest life-history stages and result in the patterns of association observed
by Queenborough et al. (2007).
Comita, Condit & Hubbell (2007) showed that the habitat
associations of adult trees might be reinforced through local
dispersal, simply due to the greater numbers of reproductive
adults present in the preferred habitat, and this increased local
dispersal could overwhelm other negative effects that adults
are hypothesized to have on nearby juveniles (Janzen 1970;
Connell 1971; Wright 2002). Local associations in the first or
even first few years of a plant’s life span may simply be the
result of this localized recruitment, so that one could argue that
the torus translation test cannot distinguish between a species
that disperses everywhere but only establishes in the preferred
habitat and a species that only disperses to the preferred habitat because that is where the adults are located. Although this
study only follows individuals once they have germinated and
cannot speak to processes occurring between the time of seed
dispersal and the annual seedling census period, every species
analysed here was found in all three of the habitats types and
across a gradient of each of the continuous topography measures. Because associations were equally prevalent when measured by abundance and survival rates (but not growth), these
associations reflect species filtering by the environment and not
just the legacy of dispersal patterns. However, the focus of the
Valencia et al. (2004) study on comparing species composition
among habitats does not permit more than a brief qualitative
comparison between the two sets of results. Additionally,
Valencia et al. (2004) found many species to be difficult to
characterize as specialists or generalists although their distributions clearly differed among habitats. Because trees are so
long-lived, it will be important to examine the trends in tree
mortality over longer time frames than the one-time picture of
abundance distributions they studied to better understand
whether these species have habitat preferences.
IMPLICATIONS OF HABITAT ASSOCIATIONS FOR
SPECIES DIVERSITY
Clearly, the environment can have a strong influence on young
seedling performance, which could indicate a role for niche dif-
ferentiation in the maintenance of diversity. Upwards of 90%
of species had abundance distributions or patterns of survival
exhibiting positive or negative associations with one or more
habitats during the study (Fig. 2). The cumulative proportion
of species exhibiting significant associations or performance
biases did not reach a plateau until five or more annual cohorts
of seedling recruits were included in the study, stressing the
necessity of long-term, community-wide monitoring to understand the importance and prevalence of habitat associations
for a number of species. Each additional year of observation
increased both the number of species studied and the number
of species for which habitat associations were detected (Fig. 2).
Tracking seedling performance over a number of years also
revealed that habitat associations were, for many species,
ephemeral or even variable across years (Table 2, Table S2).
This inter-annual variation sets the stage for coexistence to be
maintained through storage effects and the lottery model
where recruitment success varies with fluctuations in the environment, but long-lived adult trees survive through periods of
low recruitment and will again experience conditions favourable to recruitment success (Warner & Chesson 1985). In this
way, time represents another axis along which species might
vary in their response to the topographic habitat.
Many components of the niche that are correlated with
topography may vary through time, leading plant species to
respond differently to the same habitat in different years.
Although topography has been shown to be a useful surrogate
for many correlated resource axes (Hall et al. 2004; John et al.
2007), changes in climatic or other environmental conditions
among years may affect soil resources in variable ways (Sollins
1998), leading to differential responses of seedlings to the same
topographic habitat in different years. In addition, populations
of herbivores or pathogens might fluctuate in response to
inter-annual variation in climate, or in response to changing
characteristics of the abiotic environment or host populations.
This means that biotic interactions with natural enemies could
differ among years within the topographic habitat because of
habitat characteristics (Fine, Mesones & Coley 2004) or species
abundance (Comita et al. 2010; Mangan et al. 2010; Metz,
Sousa & Valencia 2010).
This study illustrates the widespread occurrence of habitat
associations at the seedling stage for large numbers of species
in a very diverse forest. The differential dynamics across topographic habitats observed here contrast with expectations of
neutral models where species have equivalent fitness and
stochastic fluctuations in abundance as a result of limited dispersal (Hubbell 2001). Whether the effects of these associations
are strong enough to have a lasting imprint on the composition of the adult forest requires further study. The seedling
dynamics of many species were consistent with patterns of
adult associations (Valencia et al. 2004; Queenborough et al.
2007), but dynamics of other species fluctuated or were
inconsistent so as to suggest a weak role in determining forest
composition. Further research is needed to determine whether
absent or weak associations are due to a scale mismatch
whereby seedlings respond to environmental variation at much
smaller scales than the 20 · 20 m quadrats studied here. The
2012 The Author. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100, 969–979
978 M. R. Metz
generality of adult habitat associations detected at this scale
should also be tested at larger spatial scales beyond the 50-ha
plot. It is possible that the weak effects of seedling habitat associations accumulate over repeated cycles of seedling recruitment and survival in the shaded understorey, so that the
composition of individuals filling canopy gaps is strongly
influenced by the topographic niche. Because associations
fluctuated across years, however, it is also possible that the
impact on forest composition of seedling responses to the
topographic environment is reversed or overwhelmed by other
processes at later life stages. Nevertheless, seedling habitat
associations are stabilizing mechanisms (sensu Chesson 2000)
that may make important contributions to the maintenance of
species diversity in tropical forests.
Acknowledgements
I thank the people and government of Ecuador for protecting their forests and
making them available for study. R. Valencia graciously provided the topographic information for the 50-ha plot, and I am grateful to him and all the
many people involved in the establishment and maintenance of the Yasunı́
50-ha forest plot. The Yasunı́ FDP is managed by the Pontifical Catholic
University of Ecuador and has been generously supported by the government
of Ecuador (Donaciones del Impuesto a la Renta), STRI, the US National
Science Foundation (NSF), the Andrew W. Mellon Foundation, and the
University of Aarhus of Denmark. An NSF Graduate Research Fellowship
supported me during the establishment of this project. W. Sousa, D. Ackerly,
J. Battles, R. Condit, C. D’Antonio, P. Fine, K. Harms, M. Rees and one anonymous reviewer provided very helpful comments on the manuscript. I thank
D. Armitage and M. Daugherty for discussions about GLMM analyses.
Completion of the study would not have been possible without funding from
several generous sources including CTFS and NSF (Dissertation Improvement Grant DEB-0407956, LTREB Grant EF-0614525) and the University
of California at Berkeley. For assistance with logistics and data collection,
I thank N. Garwood, R. Valencia, S. J. Wright, E. Zambrano, M. Zambrano,
J. Suarez, F. Hopkins, C. Hayden, A. Hartley, L. Zambrano, G. Grefa,
R. Grefa and P. Alvia.
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Received 15 August 2011; accepted 1 March 2012
Handling Editor: Mark Rees
Supporting Information
Additional Supporting Information may be found in the online version of this article:
Figure S1. Map of habitat types and the seedling network in the
Yasunı́ Forest Dynamics plot with illustrations of torus permutations.
Figure S2. Seedling abundance and performance by habitat type for
young-of-the-year seedling recruits.
Table S1. Focal species and morphospecies in the analyses.
Table S2. Internanual variation in habitat associations measured by
torus permutation tests.
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2012 The Author. Journal of Ecology 2012 British Ecological Society, Journal of Ecology, 100, 969–979