Interspecific Variation in Seed Size and Safe Sites in a Temperate Rain Forest
Christopher H. Lusk; Colleen K. Kelly
New Phytologist, Vol. 158, No. 3. (Jun., 2003), pp. 535-541.
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Interspecific variation in seed size and safe sites in
a temperate rain forest
Christopher H. Lusk' and Colleen K. Kelly2
'Departamento de Botdnica, Universidad de Concepci6n, Casilla 160-C, Concepcibn, Chile; 'Division of Biodiversityand Ecology, School of Life Sciences,
University of Southampton, UK
Summary
Author for correspondence:
Christopher H. Lusk
Tel: +56 41 203418
Fax: +56 41 246005
Email: clusk@udec.cl
Received: 28 November 2002
Accepted: 28 fanuary 2003
doi: 10.1046/j.I469-8137.2003.00760.x
The safe site concept could have utility in community ecology if predictive
relationships between plant traits and safe site characteristics could be identified.
Here we examine the proposal that the nature and relative abundance of safe sites
are systematically related t o seed size, in an assemblage of 17 woody species in a
temperate forest.
We compared the degree of associationof seedlings of each species with elevated
microsites, and examined life-history correlates of this variation.
Seed size explained 45% of interspecific variation in percentage of seedlings
growing on logs and other elevated substrates. Neither specific leaf area nor an
index of light requirements gave significant increases in explanatory power. Phylogenetically independent contrasts gave a similar, but weaker, relationship with
seed size. Most small-seeded species were overrepresented on elevated microsites,
whereas two large-seeded taxa were underrepresented on these substrates. Safe
sites of small-seeded species were therefore more spatially restricted than those of
large-seeded taxa, as elevated surfaces occupied only 8% of the forest floor.
Safe site differentiation may help to explain the wide range of seed size present
within many communities, as well as species coexistence in forests.
Key words: coexistence, leaf litter, nurse logs, seed mass, shade tolerance.
O New Phytologist (2003) 158: 535-541
Introduction
It is generally accepted that the processes of germination,
emergence and seedlingestablishment are critical in determining
the fate of individual plants, and hence in shaping community
dynamics (Grubb, 1977; Harper, 1977; Fowler, 1988). The
microsites that provide favourable conditions for these crucial
early processes in a given population are often discontinuous
or localised in space and time. Identification of such 'safe sites'
(Harper et a l , 1961 ) has therefore been a focus in demographic
studies (e.g. June & Ogden, 1975; Christy & Mack, 1984;
Fowler, 1988).
The utility of the safe site concept will be translatable from
demography into community ecology if predictive crossspecies relationships between plant functional traits and safe
site requirements can be clearlyidentified.The forest dynamics
literature provides abundant evidence that the seedlings of
different tree species respond differentially to the mosaic of
O New Phytologist (2003) 158: 535-541
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substrates present on forest floors (Stewart & Veblen, 1982;
Putz, 1983; Christy & Mack, 1984; Beatty & Stone, 1986;
Nakashizuka, 1989; Lusk & Ogden, 1992; Molofsky &
Augspurger, 1992). Seedlingsof some species have been reported
as largely restricted to fallen logs and other elevated substrates,
while others are abundant on undisturbed forest floor microsites covered by deep litter (Stewart &Veblen, 1982; Harmon
& Franklin, 1989; Nakashizuka, 1989; Hofgaard, 1993;
Lusk, 1995). One of the most striking examples of the 'nurse
log' syndrome was reported from Picea-Euga forests in the
Pacific North-west, where 88-97% of seedlings of the dominants are concentrated on logs (McKee et a l , 1982), which
cover a mere 6-1 1% of the forest floor (Graham & Cromack,
1982).Thus, safe sites for Picea and Tsuga can be said to occur
largely on elevated substrates in these forests, in that the sum
of differencesin seed arrival,germination, seedling emergence
and/or survivalconsistently gives rise to much higher seedling
densities on logs.
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Variation in substrate occupancy in forests has been linked
to seed size by some authors (Ng, 1978; Putz, 1983). A study
of a Chilean temperate forest (Lusk, 1995) found that
seedlings of small-seeded species were strongly associated with
elevated microsites, whereas large-seeded species were either
slightly
underrepresented on these substrates or showed no
.
clear preference. One possible explanation for this pattern is
that small-seeded species may have difficulty penetrating the
litter that accumulates on the forest floor, resulting in a heavy
dependence on elevated microsites, which tend to slough
litter (Christy & Mack, 1984). Although similar empirical
patterns have been reported elsewhere (Nakashizuka, 1989;
Lusk & Ogden, 1992; Molofsky & Augspurger, 1992), other
mechanistic explanations of the nurse log syndrome have also
been explored (e.g. Harmon & Franklin, 1989).
In this paper we show that the nature and relative abundance of species' safe sites are related to seed size in a Chilean
temperate rain forest. We compared the degree of association
of seedlings with elevated microsites for a complete assemblage of 17 woody species, and examined life history correlates
of interspecific variation in substrate occupancy. The present
paper builds on an earlier study at a similar site (Lusk, 1995)
by explicitly inserting the nurse log issue of forest ecology into
the wider context of the safe site, and provides a stronger test
by using a larger assemblage. Furthermore, in order to best
infer hnctional relationships between safe sites and plant
traits, we accounted for potential effects of phylogenetic relatedness by applying independent contrasts analyses (Harvey &
Pagel, 1991; Kelly, 1995).
Materials and Methods
Study site
Sampling was carried out in low-altitude forests (350-440 m
a.s.1.) in Parque Nacional Puyehue (40'39' S, 72'1 1' W) located
in the western foothills of the Andes in south-central Chile.
The climate is maritime temperate, with an average annual
precipitation of around 3500 mm (Almeyda & Saez, 1958).
The old-growth rain forest of the lower western slopes of the
Andes is composed exclusively of broad-leaved evergreen
species (Table 1). Seed size within the assemblage spans 4.4
orders of magnitude.
Sampling
Sampling was carried out on a series of transects run throughout
a total area of about 125 ha of old-growth forest. At sample
points spaced at random intervals (2-10 m apart) along transects,
seedlings (10-50 cm tall) were recorded in a circular quadrat
of l-m diameter. A total of 1616 points were sampled, yielding
a total of 1321 seedlings, with species representation ranging
from 21 to 341 individuals overall. One species represented by
only two individuals (Lomatia hirsuta) was discarded, as was
Pseudopanax kzetevirens, which usually establishes as an epiphyte
but occasionally appears on the forest floor.
Substrate at each sampling point was classified as 'elevated'
or 'forest floor'. Most elevated microsites were fallen logs, with
fewer stumps. Uprooting appeared to be less common than
Table 1 Measured life history traits of study species, and data showing association (+ ve or - ve) with elevated substrates
Density (m-*)
Species
Aristotelia serrata
Amomyi-tusluma
Aextoxicon punctatum
Azara lanceolata
Caldcluvia paniculata
Dasyphyllum diacanthoides
Embothrium coccineum
Eucryphia cordifolia
Fuchsia magellanica
Gevuina avellana
Luma apiculata
Lomatia ferruginea
Laurelia philippiana
Myrceugenia planipes
Notho fagus dombeyi
Rhaphithamnus spinosus
Weinmannia trichosperma
Seed mass
(mg)
Light requirements
(% canopy
openness)
Seedling
SLA
(cm2g-I)
Total
no. of
seedlings
on
elevated
sites
%
Association
with elevated
sites
Elevated
sites
Forest
floor
1
Light requirements represent the light environment in which juveniles of each species attain their highest density in the understorey (C.H. Lusk
Hofmann, unpublished).
& C.
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reported in some temperate forests (Beatty & Stone, 1986;
Nakashizuka, 1989), with the result that recent tip-up
mounds and pits were uncommon. The few mounds that
were encountered were classified as 'elevated', and pits were
grouped with forest floor microsites.
A pair of LAI-2000 canopy analysers (Li-Cor, Lincoln,
Nebraska) was used to quantify light environments at sampling points. One instrument was used to take measurements
at each sampling point, while the other, placed at the centre
of a 2-ha clearing, was programmed to take readings at 30section intervals. Integration of data from the two instruments
enabled estimation of percentage diffuse nonintercepted irradiance at each sampling point within the forest, equivalent to
percentage canopy openness over the quasi-hemispherical
(148") field ofview perceived by the LAI-2000 sensors. Measurements with the W - 2 0 0 0 are a good surrogate of spatial
variation in mean daily photosynthetic photon flux density
within a stand (Machado & Reich, 1999). As we explain
below, these data were used to quantify species' differences in
shade tolerance.
Species traits
We examined three key traits that could potentially influence
safe site requirements: seed mass, shade-tolerance, and specific
leaf area (SLA). Seed (strictly, diaspore) mass of most species
was obtained from Donoso & Cabello (1978). For the
remainder, seeds were collected at the study site and weighed.
As logs and other elevated substrates are likely to be associated with well-lit, recently disturbed environments, differences in substrate occupancy could be partly a reflection of
shade tolerance variation. To explore this possibility, we also
examined the relationship of substrate occupancy with species
light requirements, as indexed by the light environment (%
canopy openness) in which juveniles of each species attain
their highest densities. These modal light environments were
estimated with a generalised linear model ofvariation in density in relation to canopy openness (C. H. Lusk & G. Hofmann,
unpublished data), using a p-function (Austin et a l , 1994):
density = a (openness)b (L - openne~s)~,
Eqn 1
where a, b, c, L are parameters. The value of b represents the
rate of increase in density with increasing canopy openness,
for low light conditions, while c/L represents the rate of
decrease for light ranges beyond the optimum.
As variation in SLA is often correlated with species differences in relative growth rates (Poorter & Remkes, 1990;
Cornelissen et aL, 1996; Walters & Reich, 1999), it could also
potentially influence safe site preferences, through possible
effects on the ability ofseedlings to avoid burial by litter accumulation. SLA was therefore measured on four individuals of
each species, growing in standardised light environments of
r. 10% canopy openness, as measured with the LAI-2000.
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Statistical analyses
Randomisation tests were used to determine if each species
was more or less common on elevated substrates than would
be expected by chance. Multiple regression (JMP Statistical
S o h a r e , SAS Institute Inc., Cary, NC, USA) was used to
explore relationships of seed mass, light requirements and
SLA with the degree of dependence on elevated substrates. All
of these variables were log-transformed in order to normalise
distributions and linearise relationships.
Independent contrasts analyses
In order to best infer functional relationships between safe
sites and plant traits, we also accounted for potential effects of
phylogenetic relatedness by applying independent contrasts
analyses (Harvey & Pagel, 1991; Kelly, 1995). Comparison of
results from independent contrasts and cross-species analyses
enabled us to identify biases arising from group-specific values
of a trait that would confound an inference of functional
significance in the context currently under study. That is, if
independent contrasts analyses do not show seed size to be
correlated with proportion of seedlings on elevated substrates,
then, even if cross species analysis does show such a
correlation, it would be unwise to infer from the evidence
available here that seed size is the functional determinant of
safe site use.
The phylogenetic tree used to carry out the independent
contrasts analyses for the target species (Fig. 1) was based on
Soltis et al. (2000). This tree is resolved only to family level
and relationships within the Proteaceae and Myrtaceae, which
had multiple members in the data set, followed Johnson &
Briggs (1975) and McVaugh (1968), respectively. The recent
phylogeny by Soltis etal. (2000) produced only one difference (albeit one of some consequence) from previous phylogenies in the form of the Aextoxicaceae being- moved from its
previous position within the Celastrales to a dichotomy
shared with the rosid clade (Thorne, 1993). While it would
be of interest if previous treatments had failed to identify
correctly the Aextoxicaceae as a member of a major clade on
a par with the rosids, we have an opportunity here to examine
directly the change represented by this new arrangement. We
investigated the difference between the results assuming the
correctness for the Aextoxicaceae of previous classifications based
on the complex, multigene character of floral morphology
vs the more recent three-gene phylogeny of Soltis et al. (2000).
The data were subjected to independent contrasts analyses
for continuous variables (Felsenstein, 1985; Harvey & Pagel,
1991; Pagel, 1992; Kelly, 1995) using the CAIC package
(Comparative Analysis using Independent Contrasts; Purvis
& Rambaut, 1995). Before analysis, all data were log transformed
except for percentage seedlings on logs, for which arcsin&
transformationwas applied; arcsin produced a normal distribution of contrasts where log or logits transformations (Sokal &
&
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Laurelia philippiana
i
100 3
Gevuina avellana
4
Embothrium coccineum
Lomatia ferruginea
Aextoxicon punctatum
Dasyphyllum diacanthoides
Rhaphithamnus spinosus
Y
7
Fuchsia magellanica
I I
71
Nothofagus dombeyi
Azara lanceolata
rl-
Aristotelia serrata
Euctyphia cordifolia
Caldcluvia paniculata
Weinmannia trichosperma
Fig. 1 Phylogenetic tree of 17 target species in a temperate
rainforest, southern Chile, following Soltis et a/. (2000).
Rohlf, 1995) did not. All regressions were forced through the
origin (Grafen, 1989). With seed mass as the predictor variable, in no instance did we find a significant correlation
between variable contrast and mean at node (Felsenstein,
1985). Because we performed our analyses on fully resolved
phylogenies, it was possible to use multiple regression to
determine the independent effects of other variables upon
percentage seedlings on logs.
Results
Seed mass (mg)
Fig. 2 Relationship between seed (diaspore)size and dependence of
seedlings on elevated substrates. Dotted line shows percentage
expected to grow on elevated substrates (8%)if seedlings were
uniformly distributed.
Cross-species analysis
Seed mass was strongly negatively correlated with percentage
of seedlings on elevated microsites (Fig. 2). When the independent effects of seed mass, SLA and light requirements
where examined by multiple regression, the relationship between
seed mass and microsite occupancywas strengthened (P= 0.00 1).
SLA showed a negative relationship of marginal significance
( P = 0.06), whereas light requirements had no effect on
species' dependence on elevated substrates ( P = 0.61).
Independent contrasts analyses
When the effects of phylogenetic relatedness were factored
out through independent contrasts analyses, seed mass showed
a negative relationship with the proportion of a species'
seedlings that occurred on logs (Table 2; Fig. 3). Interestingly,
the relationship was much stronger when the classification
based on the multigene trait of floral morphology was used
than in the tree consistent with the more recent three-gene
phylogeny (Table 2). Neither light requirements nor specific
leaf area (SLA) substantially increased the explanatory power
of the model (increases in r2 12.5% in both cases). In no
instance did percentage of seedlings on logs show any association with either light requirements or SLA when individual
analyses were performed (0.12 1P10.23).
Substrate associations
Discussion
Elevated sites contributed 128 (8%) of the 1616 sample
points. Six species were more common than expected on
elevated substrates, a few such as Laurelia philippiana and
Weinmannia trichosperma achieving densities as much as
10-fold higher there than on the forest floor (Table 1).Two
species, Aextoxicon punctatum and Myrceugenia pkznipes, were
significantly underrepresented on elevated microsites.
Cross species analyses showed seed mass to be highly
correlated with substrate occupancy patterns. All seven species
that were overrepresented on elevated substrates had seed
mass < 10 mg, whereas both species that were significantly less
common than expected on these substrates had seeds > 40 mg
(Table 1; Fig. 2). The relationship revealed by independent
contrasts was not as strong as that found when phylogeny was
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Table 2 Results of single factor regression analyses for each of the
phylogenies used in our analyses
Rosids and
Aextoxicaceae
(Soltis et a/., 2000)
'1.16
P
rZ
slope
Aextoxicaceae
in Celastrales
(Thorne, 1993)
3.891
0.067
0.21
-2.365
Results for the regressions of contrast arcsin& of seedlings on logs
on contrast of log (seed mass). Column titles show the two most
closely related taxa for the phylogeny in question.
Contrast log (seed mass)
Fig. 3 Regression of contrasts of percentage of seedlings on logs
against seed mass. The results displayed here are from the
phylogenetictree in which the ~extdxicaceaeis designated as most
closely related to the rosids. After accounting for the effect of
phylogenetic relationships, only seed mass showed an association
with proportion of species' seedings found on logs vs the forest floor
(F = 3.891; P=O.067; 6 =0.21; P = -2.365).
,,,,
not accounted for, but seed size still showed an association
with variation in substrate use (Fig. 3). Although only two
crude substrate categories were distinguished here, if the
proposed causal mechanism (Ng, 1978, Putz, 1983) is
correct, species of differing seed size should show a continuum
of variation in their ability to penetrate forest floor litter
(Molofsky & Augspurger, 1992).
The association ofsome species with elevated substrates did
not appear to be attributable to higher light availability there.
Although elevated substrates were on average slightly better
lit than the rest of the forest floor (geometric mean 4.6 and
3.3% canopy openness, respectively), species light requirements
were not correlated with substrate occupancy. In fact, the
species with the highest proportion (55%) of its seedlings on
elevated substrates was shade-tolerant Laurelia philippiana,
confirming a pattern reported elsewhere (Lusk, 1995). This
reflects a very weak relationship between light requirements
and seed size, as shown elsewhere in studies that have factored
out taxonomic relatedness when examining relationships
between seed size and successional status (Kelly & Purvis,
1993; Kelly, 1995).
Apart from the effects of litter accumulation, differential
retention of seeds on logs and other elevated substrates probably also influenced seedling establishment patterns (Lusk,
1995). Although the limitations of small seed reserves could
explain the relative scarcity of species such as Laureliaphilippiana and Nothofagus dombyi on litter-covered forest floor
microsites, they do not explain why two large-seeded species
(Aextoxicon punctatum and Myrceugenia planipes) were less
common than expected on elevated substrates (Table 1).
Large seeds are unlikely to lodge in crevices and moss mats on
fallen logs, and so would rarely be retained on the convex
surfaces presented by most logs and other elevated substrates. In
contrast, most of the small-seeded species are anemochorous
(Smith-Ramirez & Armesto, 1994), and their dispersal adaptations (hairs or wings)
- could favour interception of, and
adhesion to, elevated substrates.
Elevated substrates can therefore be seen as providing
doubly 'safe' sites for small-seeded species. In addition to
sloughing litter, they confer some degree of protection from
competition from seedlings of some of the larger-seeded species, which are likely to have an initial competitive advantage
(Turnbull et al, 1999). Safe site partitioning- may
. therefore
help explain the wide range of seed sizes present in this and
many other communities (Turnbull etal., 1999), despite
model predictions of a single optimal seed size for a given
environment (Smith & Fretwell, 1974; Lloyd, 1987).
Safe sites for small-seeded species were less common that
those apt for larger-seeded associates. Small-seeded species
depended strongly upon substrates of limited and discontinuous availability (8% of the forest floor) in a more-or-less
continuous matrix suitable for large-seeded species. Several
other studies in forests have found similar trends (Putz, 1983;
Nakashizuka, 1989; Lusk & Ogden, 1992; Lusk, 1995), supporting the idea of a negative correlation between seed size
and safe site abundance in forest habitats. No such consensus
emerges from comparable studies in herbaceous vegetation,
which have generally focused on relationships of seed size
with abundance of adults, rather than juveniles (Rees, 1995;
Eriksson & Jakobsson, 1998; Turnbull etal, 1999). A metaanalysis by Xiong & Nilsson (1999) showed that the inhibitory effects of litter on germination and establishment were
greater under woody vegetation than in herbaceous communities, giving less reason to expect a strong relationship
between seed size and safe site abundance in the latter.
Is safe site differentiation in forests always associated with
seed size?Although several other studies have shown this relationship (Nakashizuka, 1989; Molofsky & Augspurger, 1992;
Lusk, 1995), other patterns could arise in situations where
other selective filters besides litter influence establishment
on the forest floor, or when disturbance impedes litter
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accumulation. For example, in a floodplain forest in New
Zealand, large-seeded Prumnopitys ferruginea was one of
several species associated with elevated microsites, whereas
small-seeded Dacrycarpus dacrydioides, highly tolerant of
inundation, grew mainly on the forest floor (Duncan, 1993)
where deep litter accumulation may have been prevented by
frequent minor floods.
In conclusion, we found that seed size was systematically
related to the nature and relative abundance of safe sites for a
complete assemblage of woody species in a temperate forest.
Although this variety of safe sites is largely a product of disturbance, interspecific variation in responses did not appear
to be linked to canopy openness, and leaf litter accumulation
patterns seem likely to be the single most important factor
mediating- the relationship between seed size and safe site
availability. This paper builds on earlier work at a similar site
(Lusk, 1995), providing stronger evidence by using a more
quantitative basis for distinguishing between the effects of
light and substrate availabilities, and by factoring out phylogeny in a larger species assemblage. Findings point to a role for
safe site differentiation in species coexistence in forests
(Grubb, 1977), and in explaining the wide range of seed size
present within many communities.
Acknowledgements
Thanks to FONDECYT for financial support through
project 1980084, and to Michael Bowler for discussion on
'forcing the origin' in independent contrasts analyses.
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Interspecific Variation in Seed Size and Safe Sites in a Temperate Rain Forest
Christopher H. Lusk; Colleen K. Kelly
New Phytologist, Vol. 158, No. 3. (Jun., 2003), pp. 535-541.
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