Biological Conservation 117 (2004) 509–519
www.elsevier.com/locate/biocon

Edge eﬀects on recruitment of Trillium camschatcense in small
forest fragments
Hiroshi Tomimatsu, Masashi Ohara*
Laboratory of Ecology and Genetics, Graduate School of Environmental Earth Science, Hokkaido University, Sapporo 060-0810, Japan
Received 4 March 2003; received in revised form 25 August 2003; accepted 27 August 2003

Abstract
To evaluate edge eﬀects on recruitment of the understory perennial herb Trillium camschatcense, spatial distribution and stageclass structure based on four life-history stages were investigated within a small forest fragment in eastern Hokkaido, Japan.
Seedlings were most aﬀected by edge eﬀects. The density of seedlings was considerably lower in the forest edges than in the interiors
and was higher on the northern side of the forest. Although three stages suﬀered edge and orientation eﬀects, ﬂowering plants
experienced much more moderate edge eﬀects than juvenile stages and showed relatively uniform distribution. The results suggestthat the recruitment of juvenile stages was strongly limited near forest edges. Seedling density was correlated with microclimaticconditions, not with seed production. The edge and orientation eﬀects on stage-class structures were also observed in two othersmall populations, emphasizing the role of edge-related decreases in seed germination and subsequent survival for limiting therecruitment of small, fragmented populations of T. camschatcense.
# 2003 Elsevier Ltd. All rights reserved.
Keywords: Edge eﬀects; Edge orientation; Forest fragmentation; Seedling recruitment; Demographic structure

1. Introduction
Forest fragmentation yields a large number of small
forest remnants. One of its important consequences is adramatic increase in edges (reviews by Lovejoy et al.,
1986; Saunders et al., 1991; Murcia, 1995), where many
physical conditions are often altered. Forest edges, forexample, are characterized by higher air and soil temperatures; and lower relative humidity and soil moisturethan forest interiors (Kapos, 1989; Matlack, 1993;
Young and Mitchell, 1994; Chen et al., 1995). Therefore,
small forest fragments are exposed to great changes in
microclimatic conditions (Kapos, 1989; Didham and
Lawton, 1999) because they have high proportions ofedges.
An altered microclimatic environment around forest
edges could directly inﬂuence plant reproduction andrecruitment (Powell and Powell, 1987; Ferreira andLaurance, 1997; Laurance et al., 1998a,b; Jules andRathcke, 1999; Mesquita et al., 1999; Restrepo and Vargas,
1999; Sizer and Tanner, 1999; Meiners et al., 2002). For* Corresponding author. Fax: +81-11-706-4525.
E-mail address: ohara@ees.hokudai.ac.jp (M. Ohara).
0006-3207/$ - see front matter # 2003 Elsevier Ltd. All rights reserved.
doi:10.1016/j.biocon.2003.08.010

instance, in Amazonian rain forests, the rate of treemortality was sharply elevated especially within 100 mof forest edges, which was assumed to result from
abrupt shifts in microclimatic conditions (Ferreira andLaurance, 1997; Laurance et al., 1998a; Mesquita et al.,1999). Instead, the recruitment of pioneers and secondary species increased (Laurance et al., 1998a,b; Sizer
and Tanner, 1999), indicating that edge eﬀect is a major
factor that changes the composition of tree communities
in this region (Laurance et al., 1998a). The recruitmentof plants around the edges can also be aﬀected indirectly through the modiﬁcations of biological interactions such as pollination (Powell and Powell, 1987), seed
predation (Jules and Rathcke, 1999), and herbivory(Restrepo and Vargas, 1999).
Plant responses to anthropogenic forest edges,
however, are not fully understood. The net eﬀects on
recruitment through the direct and indirect processes
can be either positive or negative, and therefore vary
among species (Harris, 1988). Moreover, in the temperate zone, the situation could be more complex thanthat in the tropics because microclimatic edge eﬀects
are strongly inﬂuenced by edge orientation (Matlack,
1993; Young and Mitchell, 1994; Chen et al., 1995). At

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mid- to high-latitudes in the northern hemisphere,
north-facing edges receive low solar radiation. Thus,
microclimatic edge eﬀects at north-facing edges are
weaker than at edges facing other directions (Matlack,
1993; Chen et al., 1995). However, despite the many
concerns over forest fragmentation and edge formation,
few studies have addressed how plant species are inﬂuenced by edge orientation, as well as distance from theforest edge (Wales, 1972; Matlack, 1994; Gehlhausen etal., 2000). More vigorous investigations on edge eﬀects
including the orientation perspective are required tounderstand plant responses to fragmentation in thetemperate zone.
Trillium camschatcense Ker Gawler (Trilliaceae) is along-lived herbaceous perennial common to the understory of the mesic, broad-leaved deciduous forests
throughout Hokkaido, Japan. In the Tokachi plain ofeastern Hokkaido, T. camschatcense has recently
experienced extensive habitat loss because of large-scale
agricultural development, and is now often found in theunderstory of small remnant forests surrounded by
pastureland or agricultural ﬁelds. In a previous study(Tomimatsu and Ohara, 2002), we demonstrated using
14 populations that small populations produced fewer
seeds than large populations, although the relationshipbetween population size and seed production was signiﬁcant only in one of two study years. We also showedthat seed production was related to some landscapeconditions that surround a focal population. While
many factors aﬀected the level of seed production infragmented populations as such, demographic structures based on life-history stages had strong correlations
with population size but not with the number of seeds
produced; that is, seedling recruitment was more limited
in smaller populations. We then inferred that seed production was unlikely to contribute much to subsequentdemography (Tomimatsu and Ohara, 2002). Because
small populations, which typically grow in small forest
remnants, have high proportions of edges, edge-relatedchanges in abiotic and biotic environments may provide
better explanations for low seedling recruitment in small
populations.
Here we investigate edge eﬀects on recruitment of
T. camschatcense in small fragments of cool-temperate
deciduous forest. (1) We assessed the spatial distributionof T. camschatcense individuals from diﬀerent lifehistory stages along six transects established within asmall forest fragment to see if the distribution of eachstage shows edge eﬀects, and if the extent of eﬀects
depends on edge orientation. (2) We also quantiﬁed seedproduction and microclimatic conditions that might
aﬀect recruitment of T. camschatcense to see if theyshow edge eﬀects, and if they show any spatial patterns
associated with the distribution of T. camschatcense. (3)To examine the importance of edge eﬀects in determining
demographic structure (especially seedling recruitment)in small populations, we further compared the stageclass structures in forest edges and interiors with thoseof other small fragments.

2. Methods
2.1. Study species
Trillium camschatcense, correct name for T. kamtschaticum Pall. (Fukuda et al., 1996), is an understory
perennial herb commonly found throughout Hokkaido,
Japan. This plant has four growth stages: seedling, oneleaf sterile, three-leaved sterile, and ﬂowering (Ohara
and Kawano, 1986b). It takes more than 10 years for aseedling to become a ﬂowering plant with a gradualyearly increase in leaf size, and after reaching ﬂowering,
the plants can live for at least 20 years. A ﬂowering
plant sometimes returns to its three-leaved sterile stage
the following year, possibly because of impaired photosynthesis (Ohara and Kawano, 1986b). Stems and leaves
emerge annually in late April to early May from theunderground rhizome. In the Tokachi plain, T. camschatcense ﬂowers during mid- to late May before theleaf expansion of canopy trees and has mature fruit by
the end of July. No clonal reproduction occurs in thisspecies (Ohara and Kawano, 1986a). Populations in theregion are self-incompatible and seed production resultsfrom obligatory outcrossing by insect pollination(Ohara et al., 1996). Most reproductive plants have one
or two ﬂowers. The showy white ﬂowers are visited by awide range of insects, primarily by Coleoptera (e.g.
Epuraea spp.) and Diptera (e.g. Scatophaga stercoraria)
species (Ohara et al., 1991; Tomimatsu and Ohara, inpress). A mature fruit produces  80 seeds on average(Tomimatsu and Ohara, 2002). Each seed produced has
an elaiosome, which is twice the size of the seed. Therefore, the seeds are attractive to ants, which consequently
contribute to seed dispersal (Ohara and Higashi, 1987).
2.2. Study populations
The study was conducted in the Tokachi plain ofeastern Hokkaido, Japan. Out of the 14 populations
investigated in this series of studies (Tomimatsu andOhara, 2002, 2003), the Kiyokawa population(42 450 2200 N, 143 60 5200 E; elev. 149 m) was selected forthis study. Unless otherwise noted, the experiments wereconducted using this forest fragment. The population
grows in a small (approximately 0.8 ha, a size typical inthis region), cool-temperate deciduous forest, which is
350 m apart from other large forest remnants. The sizeof this population, deﬁned as the estimated number of
ﬂowering plants, was 10,200, while the size of the other13 populations used in our series of studies ranged from4 to 153,600. The site is bordered on the northwest by a

H. Tomimatsu, M. Ohara / Biological Conservation 117 (2004) 509–519

10-m wide paved road followed by pastureland and on
the other directions by agricultural ﬁelds (Fig. 1). The
area over  10 m from the southwest-facing edge into
the forest was ploughed up for the adjacent ﬁeld,
resulting in an artiﬁcial mound where no T. camschatcense individuals were found. However, the topography
within the forest is generally gentle and no treefall gap
was found during the course of this study. The vegetation was cool-temperate deciduous forest, dominated by
Ulmus davidiana var. japonica and Fraxinus mandshurica
var. japonica. To investigate abiotic and biotic environmental gradients within the forest, six transects (A–F)
that cross at right angles were established (Fig. 1).
In this region, intensive agricultural development
began in the 1880s and has resulted in a large number offorest remnants, many of which are smaller than 1 ha.
Although the detailed history of the forest remnant isunavailable, a series of recent aerial photographs hasrevealed that the southwestern side of the study forest
was logged 20–30 years ago. The other edges were most
likely created 60–100 years ago, according to the development history of the region. The edges could be clearlydeﬁned as the location where the environment abruptly
changes due to the creation of the road or the ﬁelds.
2.3. Spatial distribution and stage-class structure
In May 2000, data sampling was carried out every 10 m
along all six transects (0, 10, 20 m,. . .). Additionally, data
were collected at 85 m points for transects C and F (i.e.,edges; Fig. 1). Six 11 m quadrats were randomly established around each sample point and all T. camschatcense
individuals were classiﬁed into one of the four stage-classes(i.e., seedling, one-leaf sterile, three-leaved sterile, and511

ﬂowering). We excluded sample points on the southwestfacing edge because no T. camschatcense individual was
found there due to the artiﬁcial mound mentioned previously. In total, we examined 55 sample points and 330
quadrats. The stage-class structure was determined for eachsample point as the relative frequency of each stage-class.
2.4. Seed production
In 1999, seed production was evaluated for individuals
found on two transects (B and E; Fig. 1), intersecting at
almost the center of the forest. Not to interfere with thesurvey of spatial distribution, measurements were madeevery 10 m along these transects, starting from a sample
point at 5 m (5, 15, . . ., 85 m). At each point, we established a 55 m quadrat. Flowers (7–27; total N=285)
within the quadrat were randomly selected, marked
before anthesis in early May, and left in an open-pollinatedcondition. Individuals with single-ﬂowering stems were
sampled for this study; however, the number of seeds produced per ﬂower showed no signiﬁcant diﬀerence between
plants with diﬀerent numbers of ﬂowering stems (H.
Tomimatsu and M. Ohara, unpublished data). All fruits
were collected from the marked individuals in July, and thenumber of seeds was counted for each fruit under a stereomicroscope. For each quadrat, fruit set and the number ofseeds per ﬂower were calculated.
2.5. Microclimatic conditions
Three variables—air temperature, soil temperature, andsoil moisture—were measured for all six transects in 2000.
Air and soil temperatures were measured at 5-m intervals
along the transects and soil moisture was measured at 10-mintervals. All measurements were made before (late May;ﬂowering period) and after (mid July; fruiting period) the
canopy closure. Air and soil temperatures were measured
with digital thermometers (NT-220, NT Corporation,
Japan; precision 0.1  C) 1.3 m above the ground and 10 cm
into the soil. We selected three sunny days for each of thetwo sample periods and measured successively during thedaytime [10.30–15.30 hours JST (Japanese Standard
Time)]. Soil moisture was gravimetrically measured
by collecting soil samples (with two replicates) with asoil-core sampler (5 cm in diameter5 cm in depth)
from the soil surface. For each sample period, samples
were collected in a single day at least 2 days after rainfall.
2.6. Statistical analysis

Fig. 1. Map showing the Kiyokawa population in the Tokachi plainof eastern Hokkaido, Japan, and the six transects (A–F) within the site
for edge eﬀects experiment.

The following analyses of spatial distribution of
T. camschatcense were conducted based on the meansof six quadrats per sample point. For the analysis ofedge eﬀects, the distance from the nearest forest edge
was determined for each sample point. The distance wasmeasured directly to the nearest edge, not along a

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transect. The signiﬁcance of edge eﬀects on the numberof T. camschatcense individuals in each stage-class wastested by regressing the number of individuals to the
distance from the nearest forest edge. In addition,
response surface regression (SAS Institute, 2000) was
performed on the number of individuals in each stageclass. Every sample point is indexed by its spatial
coordinates (x, y; Fig. 1) and a regression model isquadratic: z=a+bx+cx2+dy+ey2+fxy, where z is thenumber of individuals. The resulting response surfaces
visually characterized the patterns of edge eﬀects. The
eﬀects of edge orientation were evaluated by comparing
observed values between points around edges facing
diﬀerent orientations and by response surfaces.
Edge eﬀects on stage-class structures were analyzed asfollows. Tests of relative frequencies of all four stageclasses would not allow for statistical independence,as frequencies of any three stage-classes determine frequency of the fourth. We therefore employed a log-linear analysis for frequency tables, where the frequencies
are the number of individuals involved (Caswell, 2001).
First we placed all sample points into four discrete
categories based on the distance from the nearest forestedge (04x < 10, 104x < 20, 204x < 30, x530 m) andthen produced a three-way contingency table classiﬁed
by life-history stage (four stage-classes), transect (A–F),
and distance from the edge (four categories). We added
0.5 to all cells to avoid estimation problems of cells withzero observations. The null hypothesis is that the numberof individuals in each life-history stages (S) are independent of transect (T) and distance from the edge (D). The
complete, saturated model islog mijk ¼ u þ uTðiÞ þ uDðjÞ þ uSðkÞ þ uTDðijÞ þ uTSðikÞ
þ uDSðjkÞ þ uTDSðijkÞ
where mijk is the count in the three-way contingency
table. Each eﬀect was examined by comparing thegoodness-of-ﬁt G2 of two models that diﬀer in the terms
corresponding to the eﬀect under consideration (Proc
CATMOD; SAS Institute, 1999). The eﬀects of transect
and distance from the edge can be tested in two diﬀerent
ways. For example, the eﬀect of transect was tested withmodels including or excluding the eﬀect of distance fromthe edge. The eﬀects of edge orientation were also
analyzed by the log-linear analysis (see below).
The signiﬁcance of edge eﬀects on seed production
and microclimatic variables were analyzed by regressing
each variable to the distance from the nearest forestedge. To examine the relationships between microclimatic conditions and the spatial distributions ofT. camschatcense, we calculated Pearson’s correlations
between microclimatic variables and the number of individuals in each stage-class. Where necessary, the data were
log-transformed to meet the assumptions of analyses.

2.7. Comparison of stage-class structures with otherfragments
We further compared the stage-class structures inforest edges and interiors with those of two other small
fragmented populations, Toyonishi (42 480 1100 N,
143 90 900 E; elev. 114 m; population size 2200) andMotoimatsu (42 480 1800 N, 143 60 4300 E; elev. 120 m;
population size 18,000), of which the shape and orientation are similar to those of the Kiyokawa population.
On the basis of the aerial photographs and development
history, the edges of these fragments were most likely
created 60–100 years ago [see Tomimatsu and Ohara(2002) for further details of these populations]. In each
population, nine 11 m quadrats were established forthree categories of plot type: forest interiors ( > 20 mfrom forest edges), southern edges (410 m from southfacing edges), and northern edges (410 m from northfacing edges). All T. camschatcense individuals within thequadrats were counted and the stage-class structure wasdetermined for each plot type as the relative frequency ofeach stage-class. The diﬀerences in relative frequenciesof stage-classes among plot types and populations
were tested by the log-linear analysis. The data of theKiyokawa population were also extracted, categorized
into the three plot types, and included in this analysis.

3. Results
3.1. Spatial distribution and stage-class structure
We counted 6586 T. camschatcense individuals for all
330 quadrats of 1 m2 (Fig. 2). The number of seedlings,
one-leaf steriles, and ﬂowerings were positively related
to distance from the nearest forest edge (least-squarelinear regressions; df=1, t=4.86, P < 0.001 for seedling; df=1, t=2.14, P < 0.05 for one-leaf sterile; df=1,
t=3.12, P < 0.01 for ﬂowering), indicating that thesegrowth stages were reduced in the forest edges. Response
surface models were also signiﬁcant in these three stages(Table 1). By contrast, the number of three-leavedsteriles did not show signiﬁcant relation to distance fromthe nearest forest edge (df=1, t=0.10, P=0.92). The
response surface model also did not signiﬁcantly diﬀer
from the null model (Table 1).
The resulting response surfaces comprehensively
showed the patterns of edge and orientation eﬀects andalso the diﬀerences of those eﬀects among the threestages (Fig. 3). The number of seedlings was predicted
to be highest on the northern side of the forest (x=36,
y=58; Fig. 3) rather than the center, and reduced toward
the edges. This reﬂects the fact that the number of seedlings in almost all the transects (except F) were highest on
the northern side of the forest (approximately 70 m fromthe southwest- or southeast-facing edges), not in the

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513

Fig. 2. Number of Trillium camschatcense individuals from four life-history stages (seedling, one-leaf sterile, three-leaved sterile, and ﬂowering) per 1
m2 along six transects (A–F) established within the Kiyokawa population. The data for transects A–C and D–F are separately drawn and the peakof the number of individuals is indicated for each transect. For transects A–C, the data for the sample points at 0 m could not be obtained because of
the artiﬁcial mound (see text).

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H. Tomimatsu, M. Ohara / Biological Conservation 117 (2004) 509–519

Table 1Results of response surface analyses for the number of Trillium
camschatcense in each stage–classParameter

df

t

P

2

Seedling (R =0.45)
x
y
x2
y2
xy

1
1
1
1
1

2.00
1.80
4.34
4.35
1.26

0.05
0.08
<0.001<0.001
0.21

One-leaf sterile (R2=0.25)
x
y
x2
y2
xy

1
1
1
1
1

1.52
2.37
1.78
2.72
0.03

0.14
<0.05
0.08
<0.01
0.97

Three-leaved sterile (R2=0.04)
x
y
x2
y2
xy

1
1
1
1
1

0.69
0.91
0.36
0.24
0.92

0.49
0.37
0.72
0.81
0.36

Flowering (R2=0.29)
x
y
x2
y2
xy

1
1
1
1
1

1.24
2.25
2.64
3.12
0.39

0.22
<0.05
<0.05
<0.01
0.70

The quadratic models using spatial coordinates (x, y; Fig. 1) wereﬁtted. Estimated response surfaces are shown in Fig. 3. Analyses wereconducted for the data obtained in the Kiyokawa population.

middle of the transect (Fig. 2). Fig. 2 also shows that thetransects established on the northern side (A and D)
had higher peaks than those established on the southernside (C and F). At edges, the number of seedlings wasmuch less (43 individuals/m2).

Although the results for one-leaf steriles showed thesame trend, the edge eﬀects were somewhat weaker thanthose for seedlings (Fig. 3). Instead, the eﬀect of edge
orientation was more emphasized in the response surface than the eﬀect of forest edges. As with the seedlings, the number of one-leaf steriles was predicted to behighest on the northern side of the forest (x=33, y=64;
Fig. 3). Edge eﬀects experienced by ﬂowerings wererather weak (Fig. 3). The diﬀerences in the number of
ﬂowerings between the forest edges and interiors were
not as large as those of seedlings and one-leaf steriles(Figs. 2 and 3). However, the number of ﬂowerings was
also predicted to be highest on the northern side of theforest (x=36, y=62; Fig. 3).
Stage–class structure deﬁned as the relative frequencyof each stage-class was related to the distance from thenearest forest edge (Fig. 4). The relative frequency ofseedlings was low in the forest edges and increased withthe distance from the edge. Conversely, the frequency of
three-leaved steriles was high in the forest edges. Thesechanges in stage-class structures with distance from theedge were corroborated by the log-linear analysis(Table 2). The number of individuals in each stage-classwas not independent of transect and distance from thenearest forest edge (df=69, G2=555.73, P < 0.001). The
eﬀect of distance from the edge was signiﬁcant bothwhen the eﬀect was evaluated independently and whenthe eﬀect of transect was included in the model (Table 2).
The eﬀect of transect was signiﬁcant when the eﬀect wasevaluated independently and when the eﬀect of distancefrom the edge was included in the model. The results
showed that the relative frequencies of four stage-classes
were signiﬁcantly aﬀected by those factors. The diﬀerences among transects may reﬂect the orientationeﬀects. In fact, the frequency of seedlings were lower
and the frequency of three-leaved steriles were higher inthe southern edges than in the northern edges (Fig. 5A).

Fig. 3. Response surfaces of the number of Trillium camschatcense in each stage–class. The model for the three-leaved sterile stage did not diﬀer
from the null model (Table 1), so that the response surface was not shown. An interval between grids of response surfaces is 10 m. The point where
the number of individuals was predicted to be highest by the model is indicated by a cross (). Shaded areas indicate the forest fragment (Kiyokawa
population).

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515

Fig. 4. Relative frequency (mean of sample points+1 S.D.) of eachstage-class of Trillium camschatcense found in each of four categories
of distance from the nearest forest edge.
Table 2Log-linear analysis testing the eﬀects of transect (T), distance from thenearest forest edge (D), and their interaction (TD) on the number ofTrillium camschatcense in each stage–class (S)Eﬀect

Contrast of modelsa

df

G2

P

Transect (T)Distance (D)Transect (T),given distance
Distance (D),given transect
TD

TD, S vs. TD, TS
TD, S vs. TD, DS
TD, DS vs. TD, TS, DS

15
9
15

83.77
279.9652.37<0.001<0.001<0.001

TD, TS vs. TD, TS, DS

9248.56<0.001

TD, TS, DS vs. TDS

45

223.40<0.001Analysis was conducted for the data obtained in the Kiyokawa
population.
aNotation denotes hierarchical models in which the presence ofan interaction means the presence of all lower-order interactions
involving those variables (Caswell, 2001, Chapter 3). Thus, TDS
means the saturated model which includes all possible terms.

These analyses of stage-class structure showed that theforest edges were characterized by the low frequency ofseedlings and high frequency of three-leaved steriles.
3.2. Seed production
Fruit set and the number of seeds per ﬂower ofT. camschatcense varied among the sample points on the
two transects, B and E. The number of seeds per ﬂower,
which was employed as an index of total seed production, varied from 10.7 5.4 (mean S.E.) (B, 75 m) to109.2 12.5 (B, 25 m). In spite of the microsite variability, neither indices of seed production showed any
systematic relationship with distance from the nearest
forest edge (least-square linear regressions; df=1,
t=0.14, P=0.89 for fruit set; df=1, t=0.25, P=0.81
for number of seeds per ﬂower).

Fig. 5. Comparison of stage–class structures in the Kiyokawa
population (A) with those of two other populations, Toyonishi (B)and Motoimatsu (C). Stage–class structure was shown for each plot
type: forest interiors ( >20 m from forest edges), southern edges (410m from south-facing edges), and northern edges (410 m from northfacing edges). For the Kiyokawa population (A), relative frequency
was shown as the mean of sample points (+ 1 S.D.).

edges, and signiﬁcantly decreased with the distance fromthe edge (least-square linear regressions, P < 0.001). A
signiﬁcant positive relation was observed between soil
moisture and the distance from the nearest forest edgein May (P < 0.05), but not in July (P=0.58). However,
all microclimatic conditions in the two sample periods
were strongly positively correlated with each other(Pearson’s correlations, P < 0.05). In general, air temperature was most aﬀected by edge eﬀects and theextent of eﬀects was larger in July when the canopy had
fully developed. Air temperature also experienced theeﬀects of orientation; it was lowest on the northern sideof the forest. Soil moisture was less aﬀected.
3.4. Relationship between microclimatic conditions andspatial distribution

3.3. Microclimatic condition
All microclimatic variables exhibited signiﬁcant edge
eﬀects. Air and soil temperatures were high on the forest

Because there was no evidence that seed production
had reduced at edges, we further examined the relation of
the abundance of T. camschatcense with microclimatic

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conditions as a candidate that might aﬀect seedlingrecruitment and survival. As microclimatic conditions in
the two sample periods were strongly correlated witheach other, we used only the data in July where the edge
eﬀects were more exacerbated. The number of seedlings
was signiﬁcantly negatively correlated with air and soil
temperatures (Table 3), while the numbers of the otherstages showed no correlation with any microclimatic
variables.
3.5. Comparison of stage-class structures with two otherfragments
Although stage-class structures signiﬁcantly diﬀered
among the three populations examined, the structures in
the Toyonishi and Motoimatsu populations consistently
showed the edge and orientation eﬀects (Table 4; Fig. 5).
In both populations, the frequencies of seedlings werehighest in the forest interiors and lowest in the southernedges. The frequencies of three-leaved steriles werehighest in the southern edges and lowest in the forest
interiors. These changes in the stage-class structures
were highly signiﬁcant in the log-linear analysis(Table 4).
Table 3
Correlation coeﬃcients between microclimatic variables measured in
the fruiting period (July) and the number of Trillium camschatcense ineach stage–class (n=55)

Air temperature
Soil temperature
Soil moisture

Seedling

One-leaf
sterile

0.42
0.38
0.05

0.34
0.19
0.00

Three-leavedsterile
0.10
0.13
0.00

Flowering
0.28
0.22
0.05

Analyses were conducted for the data obtained in the Kiyokawa
population. Numbers in boldface signiﬁcantly diﬀer from zero. The
table-wide signiﬁcance was assessed using a-levels calculated according
to the sequential Bonferroni technique (Rice, 1989).
Table 4Log-linear analysis testing the eﬀects of population (P), plot type (T),and their interaction (PT) on the number of Trillium camschatcense
in each stage–class (S)Eﬀect

Contrast of modelsa

df

G2

P

Population (P)Plot type (T)Population (P),given plot type
Plot type (T),given population
PT

PT, S vs. PT, PS
PT, S vs. PT, TS
PT, TS vs. PT, PS, TS666

240.96446.54325.55<0.001<0.001<0.001

PT, PS vs. PT, PS, TS

6534.13<0.001

PT, PS, TS vs. PTS

12

50.21

<0.001Analysis was conducted for the data obtained for three populations
examined (Kiyokawa, Toyonishi, and Motoimatsu).
aNotation denotes hierarchical models in which the presence ofan interaction means the presence of all lower-order interactions
involving those variables (Caswell, 2001, Chapter 3). Thus, PTS means
the saturated model which includes all possible terms.

4. Discussion
4.1. Edge and orientation eﬀects on recruitment
T. camschatcense showed diﬀerent responses to theforest edges among the four life-history stages (Figs. 2
and 3). The density of seedlings and one-leaf steriles wasconsiderably lower in the forest edges (especially in theedges with southerly orientation) than in the interiors,
whereas the edge eﬀects experienced by ﬂowering plants
were much more moderate. The results suggest thatseedling recruitment is strongly limited around theforest edges. Because seed production did not diﬀer
between the forest edges and interiors, the distributionof seeds may not be edge-related. Although the seeds
that fell on the ground could be dispersed by ants, thedispersal distance has been reported to be short (0.60 m
on the average), up to only 3.3 m (Ohara and Higashi,1987). We also did not observe signiﬁcant seed predation. Intensive seed predation was unlikely to occur,
because large mammals such as deer, supposedly predominant predators in this region, did not have accessto the small forest isolated by large ﬁelds. Thus, it issuggested that seed germination and establishment arestrongly limited by edge eﬀects.
The density of seedlings was negatively related tosome microclimatic variables; that is, the density was
low at the sample points where air and soil temperatures
were high (Table 3). The edge environment was characterized by these microclimatic conditions, which may
be deleterious for seed germination and the establishment of T. camschatcense that normally occurs in thestable and mesic forest ﬂoor. After the fruit of T. camschatcense matures in July, the seeds require two cold
periods (normally two winter seasons) to become seedlings (Samejima and Samejima, 1962). Only the root
emerges underground after the ﬁrst cold period. Anothercold period is required for the emergence of the shoot(‘complete double dormancy’; Barton, 1944). Thus, seedlings experienced microclimatic conditions throughout
the year including the fruiting season, when microclimaticconditions may be more exacerbated. Various microclimatic changes in response to forest fragmentation canaﬀect the cues required for germination (Bruna, 1999).
The analyses of spatial distribution and population
structure made it appear that forest edges were characterized by the low frequency of seedlings and highfrequency of three-leaved steriles (Figs. 2–5). As was
discussed, low seed germination could reduce seedlingfrequency. Then, why did the frequency of three-leavedsteriles increase near edges? One possible explanation is
step-back change of ﬂowerings to the three-leaved sterile stage (Tomimatsu and Ohara, 2002). Flowering
plants that suﬀer accidental damage to their stems orleaves sometimes return to the three-leaved sterile stage
the following year (Ohara and Kawano, 1986b). Thus,

H. Tomimatsu, M. Ohara / Biological Conservation 117 (2004) 509–519

the step-back change may have also occurred due toenvironmental deterioration such as edge eﬀects. If thisis the case, the step-back change would also contributeto the slight decrease in ﬂowering plant density nearedges (Figs. 2 and 3).
As expected, this study demonstrated that edge
orientation plays a signiﬁcant role in the demography of
T. camschatcense. In particular, the recruitment ofyoung stages was clearly associated with edge orientation and was higher on the northern side of the forests(Figs. 2, 3 and 5). Although microclimatic edge eﬀects
have often been found to interact with orientation in thetemperate zone (Matlack, 1993; Young and Mitchell,
1994; Chen et al., 1995), only a few studies haveaddressed how plants respond to the forest edges facing
diﬀerent orientations (Wales, 1972; Matlack, 1994;
Gehlhausen et al., 2000). For example, Wales (1972)
showed that the eﬀects on species composition diﬀered
between edges with northerly and southerly orientations. The present study shows evidence that therecruitment of T. camschatcense is aﬀected by edge
orientation. Because the south-facing edge of the Kiyokawa population was formed more recently than theother edges, the diﬀerences in the ages of edge formation could aﬀect the results. Some studies showed thatolder edges experience milder edge eﬀects because of thedevelopment of side vegetation (Matlack, 1993, 1994).
In this study, however, it was unlikely to be responsible
because the age of the south-facing edge is > 20 years
and its side canopy closes in summer as well as in theother edges. Also, we consistently observed the eﬀects ofedge orientation in the other fragments (Fig. 5).
Two possible scenarios are proposed for the fate ofthese remnant populations, which suﬀer from strongedge eﬀects on the young life-history stages. One
scenario is that density-dependent mortality buﬀers theedge eﬀects on seedling recruitment with the progressof the stage. Because the spatial distribution of T.
camschatcense changes successively from aggregated torandom with growth from seedling to ﬂowering (Ohara
and Kawano, 1986b), the mortality may be densitydependent. This density-dependent mortality can regulate
the number of ﬂowering plants (Silvertown, 1987) andtherefore buﬀer the edge eﬀects on seedling recruitment.
An alternative scenario is that reduced seedling recruitment drives this population into decline. Because of its
long life span (at least 30 years) and the high survival
rates of ﬂowering plants (Ohara et al., 2001; H. Tomimatsu and M. Ohara, unpublished data), it is probablethat many ﬂowering plants may still have survived
fragmentation. This may be the reason why ﬂowering
plants suﬀered moderate edge eﬀects. If so, there is thepossibility that this plant species will undergo considerable losses in the next several generations. Further
demographic analyses including population projections
will be able to test these possibilities.

517

4.2. Importance of edge eﬀects in limiting recruitment
and implications for conservation
The stage-class structure in the forest edges (Figs. 4
and 5) well corresponded to that of small, fragmented
populations observed in a previous study (Tomimatsu
and Ohara, 2002). Using 14 populations with various
sizes, we previously found that seed production was
reduced in fragmented populations although stageclass population structures were not signiﬁcantly correlated with seed production but with population size
(Tomimatsu and Ohara, 2002). Speciﬁcally, smaller
populations had a lower frequency of seedlings and ahigher frequency of three-leaved steriles. Because small
populations were expected to have high proportions ofedges, the correspondence in the stage-class structures
between small populations and forest edges points to theimportance of edge eﬀects in determining population
structures (especially in limiting seedling recruitment)of small, fragmented T. camschatcense populations. The
magnitude of edge eﬀects may be related to population
size, as the distance from the center of the population to
the nearest forest edge was highly correlated with thesize of the 14 study populations (Kendall’s correlation
=0.729, P < 0.001; H. Tomimatsu and M. Ohara,
unpublished data). Although fragmented populations
also experienced reduced seed production (Tomimatsu
and Ohara, 2002), edge-related decreases in seed germination and subsequent survival, which was related tosome microclimatic variables, had higher relative
importance. The disruptions of pollination and seedproduction have been emphasized as particularly
important for population persistence especially in selfincompatible species (Rathcke and Jules, 1993; Kearns
et al., 1998); though, some recent studies (Bruna,
1999, 2002; Jules and Rathcke, 1999) and the present
study demonstrated that survival processes after seedproduction can also be crucial.
On the other hand, site eﬀects were also observed
across the three populations. The Toyonishi population
had higher frequency of seedlings than the Kiyokawa
population irrespective of its small size. This may bepartly explained by an annual ﬂuctuation of seedlingabundance and/or by inbreeding depression. Using
allozyme analysis of ﬂowering plants, we also previously
observed signiﬁcant excess of homozygotes in somesmall populations including the Kiyokawa population,
which infers signiﬁcant biparental inbreeding (Tomimatsu and Ohara, 2003). Thus, inbreeding depression
may also have reduced seed germination and subsequent survival (Oostermeijer et al., 1995; Luijten etal., 2002).
The distributions of young life-history stages (i.e.,seedling and one-leaf sterile) in the Kiyokawa population were highest on the northern side of the forest anddecreased toward the edges (Figs. 2 and 3). The result

518

H. Tomimatsu, M. Ohara / Biological Conservation 117 (2004) 509–519

obviously indicates that the small forest fragment has
no core area that is unaﬀected by edge eﬀects. Even thehighest seedling density within this fragment (27.3 individuals/m2; Fig. 2) was much lower than the mean
seedling density in a large population of 5 ha (59.2
individuals/m2; Tomimatsu and Ohara, 2002). Accordingly, seedling recruitment was limited everywhere
within the forest. It seems that edge eﬀects extended> 70 m from the southwest- or southeast-facing edges(Fig. 2). However, because this forest fragment is small,each sample point may be inﬂuenced by not only thenearest edge but also by more distant edges (Malcolm,1994). The extent of edge eﬀects would be more or lesscomplicated by these eﬀects, especially in the sample
points that are close to more than one edge. Thus thepresent study may give only limited information on how
large the distance of edge inﬂuence was.
We can at least conclude that the size of fragment of
the Kiyokawa population (0.8 ha), which is typical inthis region, is insuﬃcient to avoid signiﬁcant edge
eﬀects. The size of this population (10200 ﬂowering
plants) is much larger than those required to maintainhigh seed production (1000; Tomimatsu and Ohara,
2002) and high allelic diversity (550; Tomimatsu andOhara, 2003). Thus the eﬀects of edge orientation also
provide management implications for reserve design.
On the northern side of the forest, the density of young
stages was high in the sample points even at 10–20 mfrom the forest edges (Fig. 2). The results suggest thatedge eﬀects on recruitment can be greatly ameliorated if
the shape and orientation of remnant forests are taken
into consideration.

Acknowledgements
The authors thank E. Yamada, T. Ishibuchi, and K.
Takenaka for their help with our ﬁeld work, and M. T.
Kimura and anonymous reviewers for critical readingsof the manuscript. This research was funded in partby grants from the Sasakawa Scientiﬁc Research
Grant from the Japan Science Society, the Hokscitec
Foundation, Grants-in-Aid from the Japan Society for
the Promotion of Science (JSPS) for Scientiﬁc Research(10440230, 11691175, 13640637), and from the Ministryof Education, Culture, Sports, Science and Technology
for 21st Century CoE programs, and Research Fellowships of the JSPS for Young Scientists.

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