Journal of Ecology 2009, 97, 1037–1049
doi: 10.1111/j.1365-2745.2009.01527.x
Seedling establishment shapes the distribution of
shade-adapted forest herbs across a topographical
moisture gradient
Matthew A. Albrecht* and Brian C. McCarthy
Department of Environmental and Plant Biology, Ohio University, Athens, OH 45701, USA
Summary
1. In deciduous forests, herb distribution patterns can shift dramatically across topographical
gradients, yet it remains unclear whether topographical associations reflect regeneration niche
differences that arise during early life-history stages.
2. We examined: (i) whether seedling recruitment patterns were consistent with topographical
distributions of established populations and (ii) how environmental heterogeneity at two spatial
scales influences spatial patterns of seedling recruitment in four shade-adapted forest herbs (Actaea
racemosa, Hydrastis canadensis, Panax quinquefolius and Sanguinaria canadensis), which are
harvested from the wild for their medicinal properties but differ in life histories and seed mass.
Topographical distributions were quantified in transect surveys of forest stands, and then seed was
experimentally transplanted into litter microenvironments (bare, shallow and deep) on opposing
topographical positions (NE-facing cove forest and SW-facing oak forest).
3. Forest herbs that were more frequent in moist NE-facing cove forests (A. racemosa, H. canadensis
and S. canadensis) suffered higher mortality when their seeds were dispersed into the drier
SW-facing oak forest, although the stages that limited recruitment differed among species.
4. For A. racemosa and S. canadensis, the selectivity of the slope topographical filter varied in
strength among years that differed in soil moisture. Seedling distributions expanded across the
topographical gradient during a ‘wet’ year but contracted during a ‘dry’ year.
5. Litter effects were often context-dependent. Litter-removing disturbance increased seedling
recruitment of H. canadensis, but only in the NE-facing cove forest. When soil moisture was limiting in either space or time, microenvironments where litter was present tended to enhance
emergence and ⁄ or survival relative to litter-free microenvironments.
6. For P. quinquefolius, which has been harvested from the wild for over 200 years, seed limitation
is a fundamental constraint on its distribution along a topographical moisture gradient. Across all
microenvironments, the net recruitment rate of P. quinquefolius, the largest-seeded and least
abundant species, was an order of magnitude greater than that of A. racemosa, the smallest-seeded
and most abundant species.
7. Synthesis. Many shade-adapted forest herbs are declining in abundance due to anthropogenic
factors. Conservation efforts must consider dispersal limitation in the spatial context of environmental filters that can vary in strength and quality over time.
Key-words: Actaea racemosa, habitat limitation, Hydrastis canadensis, litter, microsite limitation,
Panax quinquefolius, regeneration niche, Sanguinaria canadensis, spatial heterogeneity, topography
Introduction
Determining the ecological factors that limit seedling recruitment is fundamental to understanding the spatial distribution
*Correspondence author. Center for Conservation and Sustainable Development, Missouri Botanical Garden, PO Box 299,
St Louis, MO 63166, USA. E-mail: [email protected]
and growth of plant populations (Grubb 1977; Harper 1977).
Dispersal results in the deposition of seeds into an array of
microenvironments that selectively filter individuals from a
pool of potential recruits (Harper 1977; Schupp 1995). The
degree to which environmental heterogeneity influences spatial
distributions can range from species whose distributional
boundaries are determined largely by environmental filters
(niche- or establishment limitation) to species whose spatial
2009 The Authors. Journal compilation 2009 British Ecological Society
1038 M. A. Albrecht & B. C. McCarthy
distributions are limited by the availability of propagules (seed
limitation) (Eriksson & Ehrlen 1992; Clark et al. 1998, 2007).
In deciduous forests characterized by strong topographical
gradients, environmental heterogeneity operates at multiple
scales and creates a mosaic of microenvironments that can
affect seedling recruitment (Whittaker & Levin 1977; Houle
1994). Slope topography generates steep and predictable gradients in light and soil moisture, and the composition of herb
communities diverges in a consistent manner across opposing
topographical positions (Whittaker 1956; Hutchinson et al.
1999; McCarthy et al. 2001; Small & McCarthy 2002; Boerner
2006). Differences in the spatial distributions of shade-adapted
forest herbs across topographical moisture gradients and forest
floor microenvironments are well described and assumed to
reflect niche differentiation (Bratton 1976; Beatty 1984;
Vellend et al. 2000). Yet, previous studies have focused almost
exclusively on the static distributions of forest herb populations (but see Vellend et al. 2000; Verheyen & Hermy 2004;
Flinn 2007), rather than on the demographic process underlying transitions from seed to established seedling when niche
differentiation and habitat associations are expected to arise
(‘regeneration niche’ sensu Grubb 1977). In long-lived forest
plants, the relative importance of seed and establishment limitation can vary across local environmental gradients and
ecological habitat preferences can change across life-history
stages (Houle 1994; Clark et al. 1998; Gómez-Aparicio 2008),
making it difficult to elucidate from static surveys how environmental factors affect the multiphase process of seedling
recruitment (Comita et al. 2007). One approach to understand
how spatial heterogeneity can structure forest herb distributions is to disperse experimentally seed across natural gradients
and explicitly link demographic processes to environmental
variation (Pulliam 2000; Flinn & Vellend 2005).
Seeds that are dispersed in a deciduous forest experience a
forest floor mosaic of litter depths that form an obvious barrier
to plant recruitment (Beatty & Sholes 1988; Facelli & Pickett
1991). A recent meta-analysis demonstrated that leaf litter
effects on plant recruitment were consistently negative in forest
ecosystems (Xiong & Nilsson 1999), as tree litter can alter germination cues (e.g. light, moisture and temperature) (Baskin &
Baskin 2001), act as a mechanical barrier to seedling emergence (Sydes & Grime 1981a; Vellend et al. 2000) and promote
soil pathogens and herbivory (Facelli & Pickett 1991). However, these ‘after-death interactions’ are seldom evaluated in
conjunction with environmental heterogeneity that is superimposed across litter gradients in natural forest communities (Eriksson 1995; Xiong & Nilsson 1999; Rinkes & McCarthy 2007).
If litter effects are analogous to plant–plant interactions, then
the magnitude and direction of litter effects could change
depending on the ecological context (e.g. water availability,
Eckstein & Donath 2005), and species identity (e.g. small versus large seeded species, Molofsky & Augspurger 1992; Eriksson 1995; Rinkes & McCarthy 2007).
In this study, we explore how environmental gradients
interact in a deciduous forest to affect spatial patterns of
seedling recruitment in four perennial herbs: Actaea racemosa (L.), Hydrastis canadensis (L.), Panax quinquefolius
(L.) and Sanguinaria canadensis (L.). We focus on these
species because they are broadly distributed in late-successional forests of eastern North America, differ in life-history traits (including seed size and seed bank longevity,
Table 1) and are declining in frequency and abundance
throughout their range (Sanders & McGraw 2002;
McGraw & Furedi 2005; Mulligan & Gorchov 2005). The
roots and rhizomes of the focal species are harvested from
the wild as a source of medicine (Robbins 2000; Albrecht
& McCarthy 2006). Conservation of these non-timber forest resources necessitates an understanding of how environmental heterogeneity structures the spatial patterns of
recruitment (Flinn & Vellend 2005; Gilliam 2007).
Table 1. Life-history features and emergence rates of the focal species
Species (Family)
Species code
Life-form
Fresh seed
mass (mg)*
Dispersal
morphology
Dispersal mode
Dispersal period
Seed bank†
Emergence
(outdoors)‡
Actaea racemosa
(Ranunculaceae)
Hydrastis canadensis
(Ranunculaceae)
Panax quinquefolius
(Araliaceae)
Sanguinaria canadensis
(Papaveraceae)
Acra
Clonal perennial herb
2.73 ± 0.06
Hyca
Clonal perennial herb
24.8 ± 1.0
Paqu
Non-clonal perennial herb
61.7 ± 0.6
Saca
Clonal perennial herb
10.62 ± 0.2
Hemispheric, brown seed
Fleshy, multi-seeded fruit
Fleshy, multi-seeded fruit
Arillate, brown seed
Gravity
August–October
Short-term persistent
16.0 ± 2.9%
Vertebrates
June–July
Short-term persistent
7.3 ± 3.0%
Vertebrates
August–October
Short-term persistent
43.3 ± 5.4%
Ants
May–June
Long-term persistent
37.3 ± 6.5%
*Estimated by individually weighing four batches of 100 randomly selected seeds.
†Data based on seed burial studies (Albrecht & McCarthy, unpublished data). Seed bank classification scheme follows Walck et al.
(2005).
‡Percentage of seeds that emerged in germination trays placed out-of-doors beneath a grove of Acer saccharum trees. Metal wire cages
were placed over trays to exclude predators and trays were checked every 10 days for two successive years.
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049
Seedling recruitment limitation in forest herbs 1039
We experimentally transplant seed into litter microenvironments of varying depths on opposing slope aspects (north-east
(hereafter NE) versus south-west (hereafter SW)) that
represent more or less the extremes of a continuum in the physical environment (i.e. light and moisture, Boerner 2006) across
the ecological range of the focal species. We focus on litter
gradients across the undisturbed forest floor because, although
decayed logs and microtopography are important sources of
environmental heterogeneity in forests, they represent only a
small fraction of microsites on the forest floor (Beatty 2003),
and the extent to which they control spatial distributions
depends largely on whether they accumulate litter (Beatty &
Sholes 1988). We tested the following predictions:
1 Forest herbs form associations with topographical
positions (if any) during the seed-to-seedling transitions
of their life cycle.
2 Mortality risk of forest herb seedlings is positively related
to soil moisture.
3 Leaf litter effects are context-dependent in that they can
alter emergence and establishment differently across
opposing topographical positions, across life-history
stages and across species.
Materials and methods
STUDY SYSTEM AND SPECIES
The four perennial forest herbs selected for study represent a range of
life-history traits (Table 1) commonly found in shade-adapted forest
herbs. Individuals of each species are potentially long-lived (up to
70 years in P. quinquefolius), and can clonally propagate from a
subterranean rhizome, except for P. quinquefolius, which typically
produces only one stem per growing season. Both P. quinquefolius
and H. canadensis are listed in Appendix II of the CITES treaty
(Robbins 2000). Each species exhibits morphophysiological seed
dormancy and therefore requires a period of warm followed by cold
temperatures before emergence occurs, which is confined to a brief
period in March–April just prior to canopy closure (Baskin & Baskin
2001). Although all four species are capable of forming persistent seed
banks (Table 1), seed dormancy of all species is broken in both light
and complete darkness (M. A. Albrecht, unpublished data; Baskin &
Baskin 2001). Thus, litter effects on seed emergence should be due to
mechanical effects, moderation of water availability, or indirect
effects (e.g. mediating seed predators), rather than to interception of
light cues (Facelli & Pickett 1991).
Study sites were located in the unglaciated Alleghany Plateau
forests of southern Ohio, USA. Approximately 70% of the landscape
is covered by secondary forest that developed following broad-scale
land clearing activities (primarily timber harvesting and grazing) at
the turn of the 19th century. This highly dissected region is characterized by repeated sequences of narrow ridge tops and stream valleys
that bracket steep forested slopes (total relief usually <150 m).
Environmental conditions covary with slope aspect, with NE-facing
slope aspects experiencing lower solar insolation levels and evapotranspiration rates, but greater soil fertility, than opposing SW-facing
slope aspects (Boerner 2006). Liriodendron tulipifera (L.) and Acer
saccharum (Marsh.) typically dominate the moist and cool NE-facing
slopes (hereafter ‘NE-facing cove forest’) and mixed Quercus communities dominate the hot and dry SW-facing slopes (hereafter ‘SW-facing
oak forest’). Graminoid abundance tends to be greater in the dry
SW-facing oak forest whereas forb abundance and diversity tend to
be greater in the cool and moist NE-facing cove forest (Hutchinson
et al. 1999; Small & McCarthy 2002).
TOPOGRAPHICAL DISTRIBUTION
We evaluated the topographical associations of the focal species using
a stratified random sampling survey of 17 second-growth forests
stands in south-eastern Ohio. Stands ranged in size from 10 to 20 ha
and were haphazardly chosen based on the following criteria: (i)
closed canopy with dominant trees >20 cm diameter and (ii) free
from obvious signs of recent large-scale disturbance such as widespread overstorey tree mortality (e.g. disease or pathogen outbreaks
and ⁄ or major ice-storm damage), and ⁄ or an understorey dominated
by disturbance-adapted, early-successional species (e.g. Rubus spp.,
Rosa multiflora).
Each stand was sampled by randomly choosing points at least
30 m from a forest edge on a ridge top. Line transects 250 m long and
4 m wide (1000 m2 or 0.1 ha) were then oriented perpendicular to the
slope aspect so that they traversed a ridge and valley system, capturing the entire topographical gradient. Each site was sampled with
three to five transects that were separated by a distance of 20–30 m
depending on stand size. Overall, 58 transects were sampled in June
or July of 2003 and 2004, corresponding to a total area of 5.8 ha or
0.058 km2. Each transect was divided into 100-m2 subplots
(25 · 4 m; 580 in total). At the centre of each subplot, we recorded:
slope aspect, slope incline (%), slope position (categorized as either
low, middle or upper slope based on percentage estimated visually of
the distance from the subplot to the nearest ridge top or valley) and
the dominant overstorey tree species. Subplots that extended into
ridge tops and valleys were considered upper and lower slopes,
respectively, since they represented <5% of the total sample; this had
no qualitative effect on the results.
We used generalized linear models (proc genmod; SAS Institute,
2001) to test for differences in the probability of occurrence (fraction
of subplots occupied) for each species across topographical gradients
using two approaches. In the first model, we used an ecological
classification scheme developed for the region (Hix & Pearcy 1997) to
assign each subplot into one of three forest types based on slope
aspect, slope position and dominant overstorey tree species: (i)
NE-facing cove forests (north-easterly aspect (316–135); slope position (lower-, mid- or upper slope); presence of one or a combination
of mesophytic overstorey trees (Acer saccharum, Liriodendron tulipifera, Fagus grandifolia and ⁄ or Quercus rubra)), (ii) transitional forests
(north-easterly aspect (316–135) or south-westerly aspect (139–
315); slope position (upper to mid-slope for north-easterly aspects
and lower slopes for south-westerly aspects); mixed-oak overstorey
tree community), and (iii) SW-facing oak forests (south-westerly
aspect (139–315); slope position (lower-, mid-, or upper slope);
mixed-oak overstorey tree community). Differences in the probability
of encountering a species in each of the three forest types were tested
using the least-square means procedure with Bonferroni-adjusted
P-values. In the second model, we linearized slope aspect values
according to an algorithm developed by Beers et al. (1966), which
assigns a value of 2.00 to an azimuth of 45 (NE) and 0.00 to an
azimuth of 225 (SW). Other azimuths are assigned intermediary
values, resulting in a continuous variable that represents a gradient
spanning dry and infertile SW-facing slopes (0.00) to moist and fertile
NE-facing slopes (2.00). We report the ‘odds ratio’ which indicates
the strength of the association for each species with the linearized
slope aspect gradient.
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049
1040 M. A. Albrecht & B. C. McCarthy
SEED TRANSPLANT EXPERIMENT
Seed transplant experiments were conducted at the Appalachian
Forest Resource Center in Meigs County, Ohio, USA (395¢ N,
829¢ W), a 20-ha second-growth forest preserve representative of
forest fragments in the broader region. This site was chosen because it
offered greater protection for potentially valuable propagules that
might be disturbed in more publicly accessed areas, and is part of a
long-term research effort to conserve and restore shade-adapted
forest herbs. Spatial distributions of the focal species were not quantified at the site, in part because the site harboured both natural and
introduced populations of the focal species, some of which were from
non-local genotypes. The distribution and abundance of natural
populations, which were known prior to introduction, were consistent with those recorded in our transect surveys of similar stands in
the surrounding region, but could have also included individuals that
had dispersed or clonally spread from introduced populations
(M. A. Albrecht, personal observation).
In a completely randomized factorial design, we established three
5.5 · 5.5 m blocks each in the NE-facing cove forest and SW-facing
oak forest, as defined previously. All blocks were located at mid-slope
positions, on moderate incline (5–15%), and in relatively uniform
canopy and microtopgraphic conditions. We chose mid- to lower
slopes because our survey results indicated that most species showed
no preference to slope position in our analysis, except for A. racemosa,
which was more frequent on mid-slope positions (see Results). We
avoided planting in areas with a dense woody understorey, which is
known to inhibit recruitment and diversity of forest understorey
plants (Beckage et al. 2000). Because the goal of this study was to
focus on abiotic gradients and litter, quadrats were cleared of all
vegetation prior to sowing seed; any vegetation that emerged
thereafter was also removed during demographic censusing. This
minimized direct (competition) and indirect (microclimate modification)
interspecific interactions that might confound interpretation of our
primary hypotheses and expanded the relevance of our study to the
ecological restoration of the focal species, since propagules are typically planted in vegetation-free patches on the forest floor (e.g.
Sanders & McGraw 2005b).
Just prior to natural dispersal, seeds of A. racemosa, H. canadensis
and S. canadensis were collected from local populations or ones
encountered in the transect surveys. Because of limited seed availability, 12-month stratified P. quinquefolius seed was purchased from an
Ohio propagator in October 2003 and sown within 15 days. For
fleshy fruited species, all pericparp tissue was removed prior to
sowing, which is commonly done before planting to reduce predation
and fungal infection. However, pre-germination treatments to simulate ingestion were unnecessary since seeds do not have physical
dormancy and germination rates are high in laboratory assays
without scarification treatments (Baskin & Baskin 2001).
We divided each block into twelve 1 · 1.5 m2 quadrats. Each
quadrat was separated by a 0.5-m buffer to minimize disturbance
during the census. For each species, 100 fresh seeds were sown in a
10-cm rectangular spacing in three randomly selected quadrats within
every block (total of 1800 seeds sown per species). Seeds were sown at
densities greater than when dispersed naturally to obtain sample sizes
that would be sufficient to detect treatment effects, since natural germination rates are often low and variable, even when predators are
prevented access to seeds (see Table 1). Because elaiosomes can affect
emergence rates of S. canadensis (Lobstein & Rockwood 1993), each
quadrat was further divided so that one half received 50 seeds with an
elaiosome and the other half received 50 seeds without an elaiosome;
elaiosomes were removed with forceps prior to planting. Seeds were
positioned at a depth of approximately 1.5 cm in the soil and litter
was re-distributed uniformly over plots to reduce predation during
the period of dormancy break to the time that litter treatment was
applied (Chambers & MacMahon 1994). Two 4 · 1 m plots that ran
parallel to both sides of all main blocks (n = 12) were established to
monitor background emergence from a latent seed bank for seeds
that might have dispersed into the area from nearby patches. No
natural recruitment was observed in these plots, thus we do not consider these transects in any subsequent analysis.
Litter depth and litter mass effects on seedling establishment are
correlated (Xiong & Nilsson 1999), so we chose litter depth as the independent variable since it is more easily measured and manipulated in
the field than litter mass. In early March 2004 before seeds emerged,
each of three species quadrats in every block was randomly assigned
to one of three litter treatments: litter removed, shallow litter (2 cm)
and deep litter (5 cm). Litter depths of 2 and 5 cm approximated the
25th and 75th quartiles of the distribution (median or 50th quartile = 3.2 cm) of leaf litter levels in transect surveys of north-easterly
and south-westerly aspects (M. A. Albrecht, unpublished data), and
represent threshold depths where litter effects can change in direction
and magnitude in many ecosystems (Xiong & Nilsson 1999). Because
germination of a single seed crop for three of the study species may be
spread across multiple years (Table 1), the same litter treatments were
reapplied to the quadrat in March 2005. In both years, seedling emergence was monitored at approximately 7- to 12-day intervals from
March to May and all new seedlings were marked with uniquely
labelled wood craft sticks. Leaf litter levels within each quadrat were
also checked and, if necessary, adjusted for uniformity within each
microsite; ‘bare’ treatments remained litter-free throughout the growing season by manually removing litter in the quadrat when necessary.
Thereafter, seedling survivorship was censused at 4-week intervals
until September, the period of above-ground senescence.
Abiotic variables were monitored concurrently over the 2-year
study period. In each quadrat, volumetric water content was
measured at each demographic census periods using a Hydrosense
moisture monitor (Campbell Scientific, Logan, UT, USA) containing
two 12-cm probes. Replicate samples (n = 3) taken within each
quadrat were later averaged for statistical analysis. All measurements
were taken ‡3 days following rainfall. During cloudy days in July
2004 and 2005, understorey light levels were quantified with hemispherical photographs taken at the centre of each plot and 1 m
in from each of the four corners (n = 5 photographs per plot).
Photographs were taken with a 35-mm Nikon digital camera (Nikon
Corporation, Tokyo, Japan) equipped with a Sigma 8-mm fish eye
lens (Sigma Corporation, Ronkonkoma, NY, USA) positioned
approximately 1 m from the ground. Digital photographs were
analysed using the Gap Light Analyzer software program to determine the absolute amount of growing season radiation (direct and
diffuse) transmitted through the canopy, after accounting for local
terrain and meteorological conditions (Frazer et al. 1999).
STATISTICAL ANALYSIS
Abiotic variables were analysed using maximum-likelihood analysis
of variance (anova) (SAS Institute 2001) with block and block nested
within slope aspect as random effects. We used a repeated-measures
mixed anova for soil moisture analysis with litter, aspect and year
considered the between-subject effects and time the within-subject
effect. For total transmitted radiation, we used a two-way mixed
anova considering aspect and litter as fixed effects.
For the seed transplant experiment, each individual seed or
seedling was considered the unit of replication. For A. racemosa and
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049
Seedling recruitment limitation in forest herbs 1041
no assumption on the distributional form of the survivor function,
hence it is considered a semi-parametric model. Aspect, litter and total
transmitted solar radiation were considered time-independent covariates, whereas soil moisture was treated as a time-dependent covariate
because values changed at each census period. We only used light data
from 2005 since there were no differences in light levels between years
(anova, P > 0.05). Block was not included in the model, as proc
tphreg is incapable of handling random effects (Allison 1995).
Probability of occurrence (mean ± SE)
S. canadensis, we analysed the two different cohorts separately in all
analyses to test for differences in first-year survival rates among years
that were characterized by dramatically different climatic conditions
and soil moisture availability. We could not examine among-year
climatic differences on H. canadensis and P. quinquefolius because
few seeds carried-over in the seed bank until 2005, and comparing
survival differences among years would have been confounded by
comparing different life-history stages (1- vs. 2-year-old seedling).
Two-way generalized linear mixed-models (proc glimmix, SAS
Institute 2001) were used separately for each species to test for
recruitment differences among litter microenvironments (three
levels) on the opposing slopes (two levels) (a total of six different
microenvironments). Block was considered a random effect and
was nested within slope aspect to account for non-independence of
seedlings in each quadrat (Littell et al. 1996). The interaction
between litter microenvironment and block was also included as
random effects. The probability of a seed emerging was modelled
as a binomial event, using a logit link function and binomial error
structure. When comparing emergence probabilities among treatments, we report the ‘odds ratio’ which, in this case, is the ratio of
the odds of a seed emerging in one microenvironment to the odds
of a seed emerging in another. Differences in seedling densities
among microenvironments at the end of 2005, which represent the
net effects of seed emergence and seedling survival, were tested
using the same generalized linear model structure with the exception that a Poisson distribution was fitted to the count data. For
both analyses, the least-square means procedure was used to
compare treatments when main effects were significant.
Although we attempted to test for cumulative survival differences
using mixed-effects maximum-likelihood methods to account for random effects and for possible non-independence of seedlings within
quadrats, some models had trouble converging due to low emergence
rates and high mortality in some microenvironments. Instead, we
tested the null hypothesis that survival among litter microenvironments was similar on the opposing topographical positions using replicated 2 · 2 contingency tables with the Mantel–Haenszel
procedure, which is less sensitive to small sample size and skewed data
(proc freq, exact test, SAS Institute 2001).
We used a modified Cox proportional hazards model (proc tphreg;
ties = discrete; SAS Institute 2001), which is capable of handling
time-dependent covariates (i.e. values that change over time) with censored survival data, to determine the relative role of litter, soil moisture and light in explaining seedling mortality. This method assumes
that explanatory variables (or covariates) are parametric, but makes
0.5
0.4
0.3
A. racemosa
a OR = 2.51
(1.91 – 3.29)
Results
ENVIRONMENTAL DISTRIBUTION
In transect surveys that spanned a variety of forest stands and
landscape gradients, A. racemosa was the most broadly distributed and abundant species in the census, occurring in 75% of
transects sampled (see Fig. S1 in Supporting Information).
P. quinquefolius was the least abundant species in the census,
averaging only 15 ramets per ha (compared to >500 ramets per
ha for A. racemosa; see Fig. S1), but was more frequently
encountered in transects (28%) than S. canadensis (22%). Frequencies of A. racemosa (F2,561=16.98, P<0.001), H. canadensis (F2,561=5.30, P=0.005) and S. canadensis (F2,561=2.72,
P<0.06) were greater in NE-facing cove forests compared to
SW-facing oak forests and transitional forests (Fig. 1), but
P. quinquefolius frequencies were consistent among forest types
(F2,561=0.36, P=0.70). Based on the odds ratios, S. canadensis
exhibited the strongest affinity for the NE-facing cove forest, as
no populations were ever recorded in SW-facing oak forests
(Fig. 1). In addition to being more frequent in NE-facing cove
forests, collective densities of A. racemosa, H. canadensis and
S. canadensis were much greater there relative to transitional
and SW-facing oak forests, although there were too many
zeroes in the data matrix for statistical analysis (see Fig. S1).
SEED TRANSPLANT EXPERIMENT
All species except H. canadensis exhibited delayed dormancy
(some seeds did not emerge until the second growing season),
which is consistent with seed burial studies that demonstrated
the potential for these species to form persistent seed banks
H. canadensis
OR = 2.22
(1.38 – 3.56)
P. quinquefolius
OR = 1.29
(0.77 – 2.16)
S. canadensis
OR = 4.06
(1.94 – 8.45)
b
0.2
a
0.1
0.0
c
a
a
b
e nal
e nal
ak
ak
ov
ov
-C nsitio W-O
-C nsitio W-O
E
E
S
S
N
N
a
a
Tr
Tr
a
a
a
b
c
k
k
e nal
e nal
v
v
a
a
o itio
o itio
-O
-O
-C
-C
SW
SW
NE rans
NE rans
T
T
Fig. 1. Probability of occurrence (mean ± SE) of forest herbs across a topographical gradient. For each species, forest types with different letters
are significantly different according to least-square means (P < 0.05). Odds ratios (±95% CL) represent the strength of association for each species with NE-facing cove forest habitat.
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049
1042 M. A. Albrecht & B. C. McCarthy
(Table 1). For seed-banking forest herbs, emergence probabilities varied across cohorts. For S. canadensis, 10.7% of seeds
emerged in 2004, whereas 5.2% of seed emerged in 2005. For
A. racemosa, 2.5% and 3.5% of seeds emerged in 2004 and
2005, respectively. Of the 470 P. quinquefolius seedlings that
emerged over two successive years, <2% delayed emergence
until 2005; thus, small sample size precluded statistical analysis
of the 2005 cohort.
We do not know the extent to which seed predators influenced the spatial patterns of emergence, although two lines of
evidence suggest background predation rates were low. First,
elaiosomes significantly enhanced emergence of S. canadensis
seedlings (Elaisome effect: F1,4 = 8.41, P = 0.01) consistently
across all microenvironments (all interactions of litter and
slope aspect with elaiosomes were not significant, P-values
‡ 0.15, see Table S1), which was unexpected since rodent seed
predators are more likely to discover buried seeds when the elaiosome is attached relative to when it is removed (Heithaus
1981). Secondly, emergence rates in germination trays that
excluded vertebrate predators were similar to or lower than
those observed in the field (see Table 1), suggesting other mortality agents are responsible for limiting emergence.
For seeds that emerged in 2004, litter microenvironments
influenced emergence probabilities but not interactively across
the opposing slopes (all Aspect · Litter interactions,
P > 0.14). Hydrastis canadensis seedlings were more likely to
emerge on NE-facing cove forest than in the SW-facing oak
forest (F1,4 = 4.76, P = 0.09), and nearly twice as likely in
0.20
A. racemosa 2004 cohort
0.15
A. racemosa 2005 cohort
NE-facing cove forest
SW-facing oak forest
0.10
Probability of emergence (mean ± SE)
bare and shallow litter microenvironments relative to deep litter microenvironments (F2,8 = 5.81, P = 0.03, Fig. 2). Emergence probabilities of P. quinquefolius seedlings were
significantly lower on deep and bare microenvironments relative to shallow litter microenvironments (F2,8 = 9.62,
P = 0.007, Fig. 2), but there were no significant aspect effects
(F1,4 = 0.05, P = 0.82).
For A. racemosa and S. canadensis, emergence probabilities
of the 2004 and 2005 cohorts varied widely across microenvironments (Fig. 2). Aspect had no effect on A. racemosa
emergence in 2004 (F1,4 = 0.18, P = 0.96), whereas the odds
of seed emerging were 3.5 times greater in NE-facing cove
forest than in the SW-facing oak forest in 2005 (F1,4 = 8.28,
P = 0.04). In contrast to the 2004 cohort, there was a significant Litter · Slope Aspect interaction on emergence probabilities of S. canadensis seeds (F2,8 = 6.72, P = 0.02) in 2005.
The odds of a S. canadensis seed emerging were 12.6 times
greater in bare microenvironments in the NE-facing cove forest than in the SW-facing oak forest in 2005 (least-square
means test: t = 3.41, P = 0.009, Fig. 2). Deep litter microenvironments consistently reduced emergence of S. canadensis
seeds relative to shallow litter microenvironments in 2005
(F2,8 = 10.53, P = 0.006), but not in 2004 (F2,8 = 0.91,
P = 0.42, Fig. 2). Similarly, shallow and bare litter microenvironments in the NE-facing cove forest increased emergence
probabilities of A. racemosa seeds relative to deep litter ones
by over 30% in 2004 (F2,8 = 3.49, P = 0.08, Fig. 2), but there
were no significant litter effects on emergence of the 2005
0.05
0.00
0.5
H. canadensis 2004 cohort
P. quinquefolius 2004 cohort
S. canadensis 2004 cohort
S. canadensis 2005 cohort
0.4
0.3
0.2
0.1
0.0
0.20
0.15
0.10
0.05
0.00
Bare
Shallow
Deep
Bare
Shallow
Deep
Fig. 2. Probability of emergence (mean ± SE) in litter microenvironments on opposing slope aspects. For 2005, emergence probabilities are conditional on the number of seeds that emerged in 2004. Probabilities are least-square means reported on an inverse link scale. Sample sizes were
too small for analysis of Hydrastis canadensis and Panax quinquefolius seeds that emerged in 2005.
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049
Seedling recruitment limitation in forest herbs 1043
Table 2. Cumulative survival (%) of the 2004 seedling cohort over
two growing seasons
NE-cove
Actaea
racemosa
Hydrastis
canadensis
Panax
quinquefolius
Sanguinaria
canadensis
SW-oak
Bare
Ambient
Deep
Bare
Ambient
Deep
33.3
15.3
50.0
33.3
30.0
25.0
36.6
19.1
18.9
15.2
21.7
23.1
68.8
62.0
62.7
34.3
60.4
58.1
42.6
35.1
46.2
16.6
26.3
17.9
A. racemosa: n = 47, H. canadensi: n = 364, P. quinquefolius:
n = 454, S. canadensis: n = 190.
(a)
Soil moisture
(c)
3
0.2
2
Ambient litter
NE-facing cove forest
SW-facing oak forest
0.0
1
0
–0.2
Parameter estimates (± SE)
–1
–0.4
–2
–3
–0.6
(b)
Light
(d) Deep litter
3
2
2
1
1
0
0
–1
–1
–2
Saca 2005
Saca 2004
Paqu 2004
Hyca 2004
–3
–2
Acra 2004
Acra 2005
Hyca 2004
Paqu 2004
Saca 2004
Saca 2005
A. racemosa cohort (litter: F2,8 = 0.83, P = 0.47; Litter ·
Aspect: F2,8 = 1.06, P = 0.39).
Even though elaiosome removal and shallow burial of
S. canadensis seeds mimic the dispersal behaviour of ants,
elaiosomes did not differentially affect spatial patterns of survival (Mantel–Haenszel procedure, all P-values ‡ 0.25) or net
recruitment (total densities) of S. canadensis seedlings (all main
and interactive effects, P ‡ 0.13), perhaps because seeds were
not deposited directly into ant nest sites or associated refuse
piles where increased nutrients may enhance establishment
(Hanzawa et al. 1988). Therefore, we combined the two seed
populations together for subsequent analyses and do not
consider elaiosome effects hereafter.
Seeds that emerged in the SW-facing oak forest experienced
total transmitted solar radiation levels that were on average
52% greater than levels in the NE-facing cove forest
(P < 0.05). Soil moisture levels were significantly greater
(Tukey–Kramer test, all P-values < 0.04) in the NE-facing
cove forest than in the SW-facing oak forest during July and
August of both years, but not during the spring emergence period (Tukey–Kramer test, all P-values > 0.14). There were no
differences in soil moisture availability among the litter
microenvironments, nor did litter effects depend on slope
aspect (see Table S2).
For seeds that emerged in 2004, survival rates after 2 years
differed among litter microenvironments on the opposing
slope aspects for H. canadensis and P. quinquefolius seedlings,
but not for A. racemosa and S. canadensis (Table 2). Cumulative survival of P. quinquefolius seedlings was similar among
litter microenvironments in the NE-facing cove forest
(v2 = 0.84, P = 0.67), but not in the SW-facing oak forest
where survival was greater in ambient and deep-litter microenvironments than in bare ones (v2 = 11.98, P = 0.003,
Table 2). Parameter estimates from the Cox regression models
indicated that litter microenvironments lowered the mortality
risk of P. quinquefolius and to a lesser extent S. canadensis
seedlings, especially in SW-facing oak forest (Fig. 3), although
Aspect · Litter interactions were not significant for either
species (Table 3). Cumulative survival rates of S. canadensis
seedlings did not significantly differ among litter
Fig. 3. Parameter estimates (±SE) from time-dependent Cox regression survival models for the following covariates: (a) soil moisture,
(b) light, (c) ambient litter and (d) deep litter. Parameter estimates for
ambient and deep litter microenvironments compare the relative risk
of dying to bare microenvironments. Positive parameter estimates
indicate that ambient and deep litter microenvironments increase the
mortality risk of seedlings compared to bare microenvironments, or
vice versa. For soil moisture and light (continuous covariates), negative parameter estimates indicate that every per-unit increase in the
covariate decreases the risk of dying, whereas positive parameter estimates indicate the reverse (see Table 1 for species codes).
microenvironments (v2 = 2.58, P = 0.29). In contrast,
H. canadensis seedling survival was lower in ambient and
deep-litter microenvironments compared to bare ones in the
NE-facing cove forest (v2 = 5.96, P = 0.05), but survival
was similar across litter microenvironments in the SW-facing
oak forest (v2 = 0.99, P = 0.61). Hydrastis canadensis
seedling survival increased as soil moisture increased, whereas
P. quinquefolius seedlings were less responsive to light and soil
moisture gradients (Table 3, Fig. 3).
For A. racemosa and S. canadensis, seedlings that emerged
in different years experienced quite different moisture conditions during the summer. Soil moisture levels were much lower
from May to August in 2005 (hereafter ‘dry’ year) relative to
2004 (hereafter ‘wet’ year), which corresponded to greater
first-year survival rates (pooled across all microenvironments)
in both A. racemosa and S. canadensis seedlings during the
wet year relative to the dry year (Fig. 4). Parameter estimates
for soil moisture were significant in the A. racemosa and
S. canadensis seedling survival models in the dry year but not
in the wet year, when growing conditions were apparently
more conducive for seedlings (Table 3, Fig. 3).
The effects of slope topography on first-year seedling
survival of the two different cohorts also differed significantly
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049
1044 M. A. Albrecht & B. C. McCarthy
Table 3. Wald’s v2- and P-values (in parentheses) from time-dependent Cox regression survival models. Models were run separately for each
species and cohort (see Materials and methods for details on model procedure). Bold values are statistically significant at P < 0.05
Species
Cohort
Aspect
Litter
Actaea racemosa
Actaea racemosa
Hydrastis canadensis
Panax quinquefolius
Sanguinaria canadensis
Sanguinaria canadensis
2004
2005
2004
2004
2004
2005
1.44
0.95
0.02
0.88
0.09
1.84
1.30
4.60
0.16
17.48
5.76
0.20
(0.22)
(0.33)
(0.89)
(0.35)
(0.76)
(0.18)
(0.52)
(0.10)
(0.92)
(0.002)
(0.05)
(0.90)
Aspect · Litter
Soil moisture
Light
–*
–*
5.62
2.27
0.92
2.40
0.03
4.23
10.23
0.93
0.24
9.31
7.89
3.61
0.01
0.01
0.38
2.04
(0.05)
(0.32)
(0.63)
(0.30)
(0.86)
(0.03)
(0.001)
(0.34)
(0.63)
(0.002)
(0.004)
(0.06)
(0.94)
(0.93)
(0.54)
(0.15)
*Effect was not included in the model because of the low number of seedlings that emerged across all litter microenvironments in the
SW-facing oak forest.
Survival (%)
100
80
60
A. racemosa 2004
A. racemosa 2005
S. canadensis 2004
S. canadensis 2005
40
20
0
Soil moisture (%)
50
40
2004
2005
***
30
***
*
20
*
10
0
April
May
Jun
Jul
Aug
Fig. 4. Cumulative first-year survival (pooled across microenvironments) of Actaea racemosa and Sanguinaria canadensis seedlings in
2004 and 2005. Bottom panel: soil moisture levels in 2004 and 2005
growing season (mean ± SE, pooled across microenvironments).
*P < 0.05, **P < 0.01, ***P < 0.001 based on repeated-measures
anova with Tukey–Kramer adjusted P-values.
among wet (2004) and dry (2005) years (Fig. 5). In July and
August of both years, soil moisture was significantly greater
(Tukey–Kramer test, all P-values < 0.04, see Table S2) in the
NE-facing cove forest than in the SW-facing oak forest,
although there were no differences in April, May or June of
either year (data not shown). Overall, cumulative seeding survival (pooled across litter microenvironments) was greater in
the NE-facing cove forest than in the SW-facing oak forest for
both S. canadensis cohorts, although the effects of slope aspect
were much more pronounced in the dry year (Fig. 5), when soil
moisture was more limiting (Table 3, Fig. 3). In contrast, firstyear seedling survival of the 2004 A. racemosa cohort was
significantly greater on SW-facing oak forest than in the NEfacing cove forest (Fig. 5) because seedling survival was positively associated with increased light levels and apparently not
limited by soil moisture (Table 3, Fig. 3). However, there were
no significant differences in survival on the opposing slope
aspects for the 2005 A. racemosa cohort, because moisture was
apparently more limiting and the positive effects of light diminished (Table 3, Fig. 3).
At the end of two growing seasons, the small-seeded A. racemosa averaged only two seedlings per plot whereas the largeseeded P. quinquefolius averaged 17 seedlings per plot (Fig. 6).
Slope aspect affected net recruitment rates of all species except
P. quinquefolius, although not necessarily equally across litter
microenvironments (Table 4). In the SW-facing oak forest,
recruitment rates of H. canadensis (Table 4) were significantly
enhanced in litter microenvironments compared to litter-free
ones (least-square means test: bare versus shallow: t = 2.48,
P = 0.04; bare versus deep: t = )2.10, P = 0.07, Fig. 4). In
the NE-facing cove forest, however, H. canadensis recruitment
rates were greater in litter-free microenvironments than in deep
litter microenvironments (t = )2.66, P = 0.03), but not
shallow litter microenvironments (t = )1.25, P = 0.25). In
contrast, P. quinquefolius recruitment rates were significantly
greater in shallow litter microenvironments than in bare microenvironments (Fig. 6), especially in the SW-facing oak forest
because of enhanced emergence and survival there (interaction
term: P = 0.12, Table 4). Seedling densities for both A. racemosa and S. canadensis were consistently greater across all litter microenvironments in the NE-facing cove forest relative to
the SW-facing oak forest (Table 4, Fig. 6).
Discussion
In eastern North American deciduous forests, slope topography creates strong environmental gradients that structure species distribution patterns and the composition of plant
communities (Whittaker 1956; Boerner 2006). Our transplant
study in an eastern North American deciduous forest suggests
that forest herbs (A. racemosa, H. canadensis and S. canadensis), which are more frequent in NE-facing cove forests,
suffered greater mortality when their seeds were dispersed into
the SW-facing oak forest, demonstrating that changes in environmental conditions across the topographical gradient can
generate different challenges for recruitment. Concordance
among patterns of seedling recruitment and the spatial distribution of populations across slope topographical gradients are
consistent with the idea that demographic processes during
emergence and establishment can shape the spatial distribution
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049
Seedling recruitment limitation in forest herbs 1045
(a)
Slope aspect
NE-facing cove
A. raceomsa
2004
SW-facing oak
A. raceomsa
2005
S. canadensis
2004
S. canadensis
2005
P = 0.24
P = 0.08
P = 0.004
100
80
60
Survival (%)
40
20
P = 0.01
0
(b) Litter
Bare
Shallow
Deep
100
80
60
40
P = 0.65
20
P = 0.29
P = 0.06
P = 0.45
0
ril ay ne ly ug pril ay ne uly ug pril ay ne uly ug pril May une July Aug
A
J
A M Ju J A A M Ju J A
Ap M Ju Ju A
Fig. 5. First-year survival of Actaea racemosa and Sanguinaria canadensis seedlings in 2004 and 2005: (a) on opposing slope aspects and (b) in different litter microenvironments. There were no significant interactions between aspect and litter for any combination of species and cohort (Mantel–Haenszel chi-squared test, all P-values > 0.08). P-values are from chi-squared tests on cumulative survival.
on seedling mortality risk indicate that soil moisture is a key
environmental factor that can limit seedling survival of shadeadapted forest herbs in the drier SW-facing oak forest. These
results are consistent with the notion that soil moisture availability is an important determinant of herb distributions along
moisture–fertility gradients that characterize hilly and mountainous regions of the deciduous forest, although to our
knowledge few studies with forest herbs have explicitly quantified and linked demographic processes along a natural soil
moisture gradient. Just as soil moisture variation in space is an
of plant populations (Grubb 1977). However, the selectivity of
slope topography as an environmental filter varies over time,
can change across early life-history transitions, and can
interact with fine-scale heterogeneity in leaf litter.
SEEDLING RECRUITMENT ACROSS ABIOTIC
GRADIENTS
For forest herbs with increased frequencies in the NE-facing
cove forest, significant parameter estimates for soil moisture
NE-facing cove forest
Net recruitment (seedlings per m2)
Bare
Shallow
SW-facing oak forest
Deep
35
30
25
20
15
10
5
0
sa sis sis
us
sa sis sis ius
sa sis sis
us
mo aden aden uefoli
mo aden aden uefoli cemo aden aden uefol
e
e
c
c
n
n
q
n
n
q
n
n
q
ra
ra
ra
A. S. ca H. ca . quin
A. S. ca H. ca . quin
A. S. ca H. ca . quin
P
P
P
Seed mass
Fig. 6. Net recruitment rates (mean ± SE, total number of seedlings in 2004 cohort + total number of seedlings in 2005 cohort) of forest herbs
across all microenvironments at the last demographic census in 2005. Seedling densities are least-square means (±SE) from mixed-model
analyses with a Poisson error distribution. Species are arranged along the x-axis from left to right in order of increasing seed mass (see Table 1 for
seed mass values).
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049
1046 M. A. Albrecht & B. C. McCarthy
Table 4. Effects of slope aspect and litter on net recruitment rates
(mean ± SE, total number of seedlings in plots at the last census) of
seed planted in 2003. Bold values are statistically significant at
P < 0.05
Aspect
Species
F
Actaea racemosa 3.37
Hydrastis
7.06
canadensis
Panax
0.17
quinquefolius
Sanguinaria
10.03
canadensis
Aspect ·
Litter
Litter
P-value F
P-value F
P-value
0.09
0.03
0.82 0.48
2.01 0.20
0.03 0.97
5.05 0.04
0.69
4.82 0.04
2.83 0.12
0.01
0.16 0.85
0.45 0.65
important axis for niche differentiation in these forest herbs,
so, too, can the effects of soil moisture on seedling survival
change across time. Overall, seedlings of A. racemosa and
S. canadensis that emerged in the drier year were more likely to
die than seedlings that emerged in the wetter year.
In addition to increasing temporal variability in seedling
establishment, changes in soil moisture across years also
altered the strength of slope topography as an environmental
filter. For seeds of A. racemosa and S. canadensis that delayed
emergence until the dry year, this imposed demographic costs
that contributed to greater net recruitment rates in the NEfacing cove forest. For A. racemosa seeds that delayed emergence, emergence rates were much lower in the SW-facing oak
forest compared to the NE-facing cove forest, probably
because seeds that remained dormant in the forest experienced
warm and dry conditions that are known to accelerate seed
desiccation and death (Baskin & Baskin 2001). Although
increased light availability in the SW-facing oak forest
enhanced survival of A. racemosa seedlings relative to the NEfacing cove forest during the wet year, seedling stress associated with lower soil moisture availability in the SW-facing oak
forest during the dry year could not be mitigated by the
increased light levels there, resulting in expansion and contraction of seedling distributions across the topographical gradient. For S. canadensis, which was strongly associated with
NE-facing cove forest habitat in transect surveys, a similar pattern of lower emergence in the SW-facing oak forest was also
observed in the dry year, but only in litter-free microenvironments. Although shallow litter microenvironments enhanced
emergence in the SW-facing oak forest during the dry year,
there were no demographic benefits for seedlings that emerged
there, suggesting that microenvironments differ in their relative
suitability at the seed and seedling stages (Schupp 1995). Differences in first-year survival of S. canadensis seedlings on the
opposing slopes were consistent across litter microenvironments (no Aspect · Litter interactions for survival or net
recruitment) in both years, but tended to be more pronounced
in the dry year relative to the wet year. We therefore conclude
that seedling establishment is the key demographic parameter
restricting S. canadensis from the SW-facing oak forest.
Emergence and establishment of P. quinquefolius was less
influenced by topographically driven gradients in soil moisture
and light than the other forest herbs, perhaps owing to its
much larger seed size. Across all microenvironments, P.
quinquefolius seedling densities were equal to or greater than
those of the other forest herbs and were a magnitude greater
than those of the smallest-seeded species, A. racemosa. In
other seed addition experiments with forest herbs, recruitment
rates for larger-seeded species are generally greater than for
smaller-seeded ones (Ehrlen & Eriksson 2000; Moles & Westoby 2002), presumably because larger seeds confer greater tolerance to hazards such as low light levels, defoliation, nutrient
shortages and intermittent periods of drought (Leishman &
Westoby 1994).
Because of difficulties sampling patchily distributed forest
herbs over large spatial scales, it remains an open question
whether P. quinquefolius forms associations with topographical gradients in our study system. For wild harvested species,
distributional patterns across environmental gradients do not
necessarily reflect the realized niche of the species, since
humans may have disproportionately harvested P. quinquefolius
from habitats where the species was historically more frequent (McGraw et al. 2003). Descriptions of P. quinquefolius
populations often identify NE-facing cove forests as the
preferred habitat, but transect surveys similar to ours have
found population frequencies and sizes that were equal to or
greater on south- and west-facing slope aspects (McGraw
et al. 2003), which is consistent with our finding of enhanced
recruitment there. However, this seemingly broad distribution across environmental gradients could be altered by the
effects of abiotic or biotic filters that change in strength
and ⁄ or quality during demographic transitions beyond
emergence and seedling survival.
ECOLOGICAL CONSEQUENCES OF LITTER
HETEROGENEITY
While litter is often conceptualized as an environmental filter
that directly or indirectly modifies the physical, chemical and
biotic environment (Facelli & Pickett 1991), recent studies
show that the magnitude and direction of litter effects on seedling recruitment are often context-dependent (Xiong et al.
2003; Eckstein & Donath 2005). The broad range of demographic responses of individual species, cohorts and life-history
stages to litter microenvironments observed here conforms to
this expectation: litter mediates emergence and establishment
of shade-adapted forest herbs, but sometimes in very different
ways across opposing topographical positions and over time.
Our results suggest that litter-removing disturbances can
expand the local distribution and abundance of H. canadensis,
but only in the NE-facing cove forest. Litter-free microenvironments in the NE-facing cove forest enhanced emergence
and survival, leading to net recruitment rates that were 10
times greater relative to litter-free microenvironments in the
SW-facing oak forest. Other studies with H. canadensis have
found that adult survival does not limit population spread
along topographic-environmental gradients (Sanders &
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049
Seedling recruitment limitation in forest herbs 1047
McGraw 2005a), consistent with assumptions of the regeneration niche concept that adults can persist in much broader
niche space than seedlings can recruit (Grubb 1977). Across
the species’ entire range, H. canadensis populations are often
distributed adjacent to rivulets, stream terraces or valley-floors
(Sinclair & Catling 2000; Meyer & Parker 2003), where localized flooding in early spring may remove litter mats and create
bare patches of soil that are known to facilitate seedling
recruitment in productive environments (Xiong & Nilsson
1999). Unlike the other forest herbs in this study, H. canadensis
seedlings produce only cotyledons rather than a true shoot in
the first-growing season, which probably limits their ability to
penetrate and dislodge thick mats of litter on the forest floor
(Sydes & Grime 1981b). These litter-free microenvironments
in the NE-facing cove forest also reduced seedling mortality
risk relative to adjacent microenvironments where litter was
present, possibly by thinning herbivores and pathogens that
can accumulate in moist litter layers of H. canadensis populations (Rock 2000).
Despite the potential benefits of a litter-free microenvironment in the moist NE-cove forest, the quality of litter microenvironments changed as soil moisture availability decreased in
space or time. Enhanced survival of A. racemosa seedlings in
deep litter microenvironments in the dry year but not the wet
year, and the tendency for P. quinquefolius seedlings to benefit
more from litter-microenvironments on the dry SW-facing oak
forest than on the moist NE-facing cove forest, suggest that
litter alleviated moisture stress via ‘mulching’ effects (Facelli &
Pickett 1991). Positive litter effects have been reported in
seasonally dry ecosystems (Becerra et al. 2004; Rotundo &
Aguiar 2005), grasslands (Fowler 1986; Nash & Goldberg
1999) and canopy gaps of tropical forests (Molofsky &
Augspurger 1992), but are seldom observed in undisturbed
temperate forests where litter effects are expected to be negative (Xiong & Nilsson 1999; but see Donath & Eckstein 2006;
Rinkes & McCarthy 2007). Although there were no detectable
differences in soil moisture across litter microenvironments
during any sample period, we measured the collective moisture
availability of a 12-cm deep profile, a scale less relevant for an
individual seed lying just below the soil surface or for a
shallowly rooted seedling (Harper 1977). Compared to litter
microenvironments, litter-free areas on SW aspects experience
warmer temperatures and lower humidity at the plant–soil
interface (McKinney 1929). Such conditions are known to
affect negatively shade-adapted forest herbs that are shallowly
rooted (Neufeld & Young 2003), but can be ameliorated by the
presence of leaf litter (Donath & Eckstein 2006).
However, forest floor microenvironments that accumulate
excessive litter depths, such as treefall pits and the bases of canopy trees, typically harbour low densities and few species of
forest herbs (Beatty & Sholes 1988), suggesting a threshold
where litter switches from facilitative to becoming predominantly inhibitive. Across ecosystems world-wide, Xiong &
Nilsson (1999) reported a quadratic relationship between litter
depth and emergence probabilities, where the facilitative
effects of litter tended to diminish at depths >1.5 cm. Even
though litter depths could not be experimentally controlled to
the same degree as in glasshouse studies, deep litter microenvironments (5 cm depth) reduced emergence relative to shallow
litter (2 cm) ones consistently on both slope aspects in many
instances of our demographic study. Litter quantities that were
inhibiting to emergence in this study are consistent with those
that reduced forest herb recruitment in treefall pits (4–5 cm
depth, Beatty & Sholes 1988) and the emergence of successional woody plants in glasshouse pots (100–300 g m)2,
Peterson & Facelli 1992).
CONSERVATION AND MANAGEMENT IMPLICATIONS
When seeds are dispersed across a range of microenvironments
and fail to recruit in some of them, then the availability of
suitable habitat can limit local plant distributions. Our study
suggests that the transition from seed to an established seedling
is an important demographic bottleneck for some shadeadapted forest herbs and can potentially shape their spatial
distributions across a topographical moisture gradient. Even if
seeds of these forest herbs are dispersed into the drier SWfacing oak forest, opportunities for seedling establishment are
often limited by soil moisture availability, and probably by
competition with more light-demanding grasses and forbs at
later life-history stages (Sydes & Grime 1981a; Beatty 2003).
As these late-successional herbs slowly re-colonize forest
stands recovering from broad-scale disturbances of the late
19th century (e.g. logging and agriculture), post-dispersal
demographic processes help explain why species–environment
relationships become increasingly important in shaping forest
plant distributions along environmental gradients (Gilliam &
Roberts 2003; Gilliam 2007; Vellend et al. 2007). Once
shade-adapted forest herbs that lack long-distance dispersal
mechanisms (ants for S. canadensis, gravity for A. racemosa)
eventually colonize a recovering forest, dispersal limitation
probably reinforces their associations with the preferred NEfacing cove forest, where much of the undisturbed forest floor
remains unoccupied but apparently suitable for recruitment.
Dispersal limitation in time and possibly space may further
limit the ability of H. canadensis to exploit litter-free patches
within the preferred NE-facing cove forest.
In contrast, our data suggest that topographic-environmental gradients in an eastern North American deciduous
forest play only a relatively minor role in limiting the local
distribution and abundance of P. quinquefolius, which has
declined dramatically in the region. Similar to other studies
(McGraw et al. 2003), our transect surveys indicate that
P. quinquefolius populations are numerically small and
infrequent, but could potentially grow and spatially expand
if filters on seed limitation (e.g. allee effects, deer browse
and human harvest) can be overcome. Because increased
rates of seed emergence can dramatically enhance P. quinquefolius population growth rates, the relatively high net
recruitment rates across a range of microenvironments
demonstrated here support models that show population
declines could be reversed over the long term through a
management programme of planting ripe seed in local
populations (Van der Voort & McGraw 2006).
2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049
1048 M. A. Albrecht & B. C. McCarthy
Our experimental demographic analysis of a small number
of shade-adapted herbs in a deciduous forest clearly show that
the relative influence of environmental gradients can change in
strength and quality from 1 year to the next. This temporal
uncoupling appears to complicate categorization of specific
microenvironments as ‘safe sites’ for seedling recruitment.
Litter microenvironments mediate spatial distributions in
some years but not others (e.g. A. racemosa), or as part of a
hierarchy of interacting abiotic and biotic factors that influence
seedling recruitment (e.g. H. canadensis). The unique
responses of individual species and life-history stages to spatiotemporal heterogeneity also suggest that life-history traits (e.g.
seed mass and seedling morphology), in combination with
niche and dispersal limitation (Gilbert & Lechowicz 2004;
Flinn & Vellend 2005), are important determinants of forest
herb distributions (also see Flinn 2007). Because temperate
forests are characterized by environmental heterogeneity at
multiple spatial and temporal scales, careful consideration of
the interactions between habitat suitability, life-history stage
and contingencies (‘year’ effects) is needed when using seed
addition (or supplementation) to restore populations and
understand the spatial patterns of forest plants.
Acknowledgements
Glenn Matlack, Jim Dyer and Phil Cantino provided valuable comments on a
previous draft of this paper. We thank Vanessa Polling, Rob Kaminski and
Travis Stevens for field assistance. We thank two anonymous referees for
comments on the manuscript. We are grateful to the staff at the Wayne
National Forest and Appalachian Forest Resource Center for logistical support throughout this project. This work was supported by USDA-SARE Grant
LNC02-221 to B.C.M. and a Ford Foundation Grant to M.A.A.
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Received 11 February 2009; accepted 5 May 2009
Handling Editor: Frank Gilliam
Supporting Information
Additional Supporting Information may be found in the online
version of this article:
Figure S1. Distribution and abundance of four forest herbs in
transect surveys of forest stands in southern Ohio.
Table S1. Mixed-model analysis on the effects of elaiosomes on
emergence rates of Sanguinaria canadensis seeds in 2004.
Table S2. Mixed-model analysis of differences in soil moisture levels
across microenvironments.
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2009 The Authors. Journal compilation 2009 British Ecological Society, Journal of Ecology, 97, 1037–1049