The effects of litter accumulation through succession on seed bank formation for small- and...

Journal of Vegetation Science && (2013)

The effects of litter accumulation through successionon seed bank formation for small- and large-seededspecies

Chika Egawa & Shiro Tsuyuzaki

Keywords

Germination traits; Grass litter; Secondary seed

dispersal; Seed viability; Seed size

Abbreviations

AIC = Akaike’s information criterion; GLMM =

generalized linear mixedmodels; PAR =

photosynthetically active radiation.

Nomenclature

Ohwi & Kitagawa (1983)

Received 28 June 2012

Accepted 26 November 2012

Co-ordinating Editor: Lindsay Turnbull

Egawa, C. (corresponding author,

[email protected]) & Tsuyuzaki, S.

([email protected]): Graduate School of

Environmental Earth Science, Hokkaido

University, Sapporo, 060-0810, Japan

Abstract

Questions: How does litter accumulation through succession affect secondary

seed dispersal and buried seed viability and consequently control seed bank for-

mation for small- and large-seeded species?

Location: A post-mined peatland in northern Japan (45°06′ N, 141°42′ E)where the chronological sequence of plant community succession is known.

Methods: The movements of seeds after reaching the ground surface and the

availability of viable seeds potentially contributing to seed bank formation at

various depths were experimentally investigated for 1 yr in four species that

produce different-sized seeds: Drosera rotundifolia (seed mass 0.01 mg), Lobelia

sessilifolia (0.25 mg), Rhynchospora alba (0.87 mg) and Moliniopsis japonica

(1.82 mg). The experiments were conducted in three successional stages with

0-, 4- and 9-cm thick litter layers.

Results: Seed emigration decreased and seed retention increased with an

increase in litter thickness. Large seeds were retained within the litter through-

out the experimental period, and fewer seeds were buried in peat compared to

small seeds trapped by thick litter, which had shifted downward by the following

early spring. Litter contributed to increasing the number of viable and ungermi-

nated seeds. The number of viable seeds for all species was nearly zero on the

bare peat surface. The numbers of viable seeds on and beneath the peat surface

increased with increases in litter cover thickness.

Conclusions: The patterns of secondary seed dispersal and the availability of

viable seeds were altered by litter accumulation through the progress of succes-

sion. Moreover, the effects of litter on seeds varied among species for which seed

size differed. Overall, our results suggest that temporal changes in litter thickness

through the progress of succession can play an important role in seed bank for-

mation, which has potential impacts on the long-term dynamics of plant popula-

tions and the whole community.

Introduction

Seed banks can be sources for the future regeneration of

plant species and have potential impacts on long-term

population dynamics (Thompson & Grime 1979; Baskin

& Baskin 1998). Therefore, detecting the mechanisms

underlying seed bank formation is essential to improve

our understanding of how plant communities develop

and are sustained. The patterns of seed bank formation

depend on seed characteristics (Fenner & Thompson

2005). For instance, species that produce small seeds

tend to form persistent seed banks in deep soil layers,

while large seeds often develop transient seed banks in

shallow layers (Thompson et al. 1993; Bekker et al.

1998). This occurs because small seeds are buried in soil

more rapidly than large seeds, and thus are more likely

to escape from hazards present at the ground surface,

such as predation, and to survive for a longer time

(Fenner & Thompson 2005). In addition to seed charac-

teristics, the physical environment can affect seed bank

formation, generating spatial heterogeneity in the seed

bank distribution for a given species (Bekker et al. 1998;

Journal of Vegetation ScienceDoi: 10.1111/jvs.12037© 2013 International Association for Vegetation Science 1

Funes et al. 2001). During the succession of a plant com-

munity, physical environments vary with changes in the

quality and quantity of standing vegetation and litter

(Miles & Walton 1993). In particular, litter often has

large impacts on seed movement, longevity and germi-

nation (Rotundo & Aguiar 2005; Ruprecht & Szab�o

2012), and plays a fundamental role in shaping plant

community structure (Xiong & Nilsson 1999). There is

no or little litter in the initial stage of succession, and lit-

ter gradually accumulates and modifies the topography

and micro-environments as succession progresses (Fa-

celli & Pickett 1991). Thus, the process of seed bank for-

mation for a species may differ among successional

stages with different amounts of litter. However, the

mechanisms underlying the temporal changes in seed

bank formation associated with litter accumulation are

poorly understood.

Litter accumulation through succession can affect seed

bank formation in two ways: modifying the ground sur-

face topography to alter secondary dispersal patterns

(Chambers & MacMahon 1994; Ruprecht & Szab�o 2012)

and changing micro-environments to affect the number

of viable seeds (Facelli & Pickett 1991). Secondary seed

dispersal, the movement of seeds after arriving on the

ground surface, often determines the fate of seeds, i.e.

regarding germination, predation and seed bank forma-

tion (Chambers &MacMahon 1994; Fenner & Thompson

2005). Because secondary seed dispersal depends on the

ground surface topography (Chambers 2000; Benvenuti

2007), litter often modifies the patterns of dispersal (Fa-

celli & Carson 1991). For example, seeds on bare ground

are easily found and removed by insects and animals, but

removal decreases with increases in litter (Vander Wall

1993). Wind promotes the horizontal movement of seeds

when vegetation and litter are sparse (Chambers & Mac-

Mahon 1994); however, thick litter restricts these move-

ments (Facelli & Pickett 1991). In boreal regions, the

large amount of snowmelt water running in early spring

also contributes to seed movements (Scherff et al. 1994).

Litter alters the flow of snowmelt water; sheet flow is

expected to occur on bare ground, but this type of flow is

prevented when litter is present. Because water carries

small seeds more readily than large seeds (Chambers &

MacMahon 1994), changes in snowmelt water flow

caused by litter are expected to alter seed movement pat-

terns, particularly for small seeds.

Litter also can affect the number of viable seeds that

potentially form a seed bank by altering the micro-envi-

ronment. Seed germination can contribute to seedling

establishment and, at the same time, can reduce the num-

ber of viable seeds in the seed bank (Hyatt & Casper 2000;

Caballero et al. 2005). Germination on and under the

ground is mainly induced by the presence of light and large

fluctuations in temperature (Burmeier et al. 2010; Saatk-

amp et al. 2011). Litter reduces both the light intensity

and temperature fluctuations (Donath & Eckstein 2010),

which can maintain seeds within or beneath litter in an

ungerminated and viable state (Rotundo & Aguiar 2005;

Wijayratne & Pyke 2012). Therefore, both secondary seed

dispersal and the input of viable seeds to the seed bank can

vary temporally with litter accumulation through the pro-

gress of succession. In addition, the effects of litter accumu-

lation on seed bank formation may differ depending on

seed size.

In this study, we examined how litter accumulation

alters seed bank formation processes in multiple species

with different-sized seeds in a post-mined peatland, the

Sarobetsu Mire, in northern Japan. In the peatland, peat

was mined annually from 1970 to 2003. The former veg-

etation, litter and seed bank in the area were completely

removed by peat mining, and succession has been pro-

ceeding from bare ground covered with peat residue (Ni-

shimura et al. 2009). Because the time since mining

operations ceased varies among sites, we can simulta-

neously observe several successional stages within the

peatland. Therefore, the post-mined area with a known

history of disturbance and subsequent succession pro-

vides a unique opportunity to investigate the effects of

litter accumulation through succession on seed bank for-

mation. Furthermore, a loose structure of peat layers

may allow detailed investigation of the vertical move-

ment of seeds. In the post-mined peatland, the distribu-

tion and persistence of the seed bank are different

among species due to their different seed sizes (Egawa

et al. 2009). In the present study, we conducted two

field experiments using four species producing different-

sized seeds to trace secondary seed dispersal and to

investigate the availability of viable seeds after 1 yr of

burial at various depths. We focused primarily on litter

thickness and not on litter quality because the former

parameter differs among successional stages, whereas

the latter does not appear to differ considerably, as most

of the dominant species in the post-mined peatland are

monocotyledons. The following hypotheses were

addressed regarding the interactions between litter

thickness and seed size in relation to the seed bank for-

mation processes: (1) seeds after primary dispersal are

more likely to be trapped in thicker litter than in thin lit-

ter layers; (2) small seeds pass through the litter more

readily than large seeds and reach the peat surface; (3)

snowmelt water contributes to the vertical movement of

small seeds, but not large seeds; (4) the number of viable

seeds increases with the burial depth and with increases

in litter thickness; and therefore, (5) seed bank forma-

tion processes differ among seeds of different sizes,

whose burial depth is determined by litter thickness.

Journal of Vegetation Science2 Doi: 10.1111/jvs.12037© 2013 International Association for Vegetation Science

Litter accumulation controls seed bank formation C. Egawa & S. Tsuyuzaki

Methods

Study site

The study site, the Sarobetsu Mire, is located in the north-

ernmost part of Hokkaido, Japan (45°06′ N, 141°42′ E,7 m a.s.l.) and spans 28 km from north to south and 5–

8 km from west to east. The development of the mire

began 4000–4500 BP after the JapanMarine Transgression

through the accumulation of Sphagnum peat (Oka et al.

2005).

Sphagnum peat was mined annually in the mire with a

large suction-type peat rig to depths of more than 3 m over

areas of 3–22 ha from 1970 to 2003 (Nishimura et al.

2009). Therefore, the former vegetation, litter and seed

bank in the area were completely removed with the peat.

After the high-quality peat was extracted, the residues

were returned to their original locations and gradually

developed a denuded peat surface. Thus, bare ground rep-

resented the initial stage of succession. This bare ground

was replaced by a Rhynchospora alba (L.) Vahl grassland,

which proceeded to a Moliniopsis japonica (Hack.) Hayata

grassland. Because the timing of the mining activities was

different among sites, several successional stages can be

observed simultaneously within the peatland. However,

the rate of succession has differed within even-aged sites,

most likely because of environmental heterogeneity (Ni-

shimura et al. 2009). Therefore, several different vegeta-

tion types can be distinguished within even-aged sites. We

addressed three representative successional stages in our

experiments: bare ground mined in 1973, an R. alba grass-

land mined in 1972 and an M. japonica grassland mined in

1972. The distances between the three sites ranged from

200 to 400 m.

The 2010 mean annual air temperature measured at a

meteorological station 6 km from the study sites in Toyo-

tomi Town was 6.8 °C, with a minimum�6.0 °C recorded

in February and a maximum of 21.9 °C in August (SDMO

2010). The annual precipitation in the same year was

1168 mm. The snow-free period usually lasts from mid-

April to mid-November. Seedlings of most species emerge

during late May and late June (Egawa & Tsuyuzaki 2011),

and the primary seed dispersal for most species occurs in

late autumn (Egawa et al. 2009).

Species and seed sources

Four common perennial species were included in the

experiments: R. alba, M. japonica, Lobelia sessilifolia Lamb.

and Drosera rotundifolia L. These species differ in the timing

of their establishment during succession. As previously

described, R. alba is the earliest colonizer of bare ground.

M. japonica follows R. alba, and L. sessilifolia and D. rotundi-

folia colonize vegetated habitats, including R. alba grass-

lands. The seed bank distribution and persistence also

differ among the four species: D. rotundifolia develops a per-

sistent seed bank, whereas R. alba andM. japonica develop

transient seed banks in the peatland when vegetation and

litter develop well (Egawa et al. 2009). L. sessilifolia devel-

ops a seed bank whose persistence remains unknown

(Koyama & Tsuyuzaki 2010).

Seeds were collected from more than 50 individuals for

each species in the post-mined peatland in autumn 2009

and kept in paper bags at room temperature until used in

experiments. Prior to the experiments, 50 seeds of each

species were randomly selected and weighed to quantify

their size. The length, width and depth of the seeds were

also measured. The seed shape was expressed based on the

variance in the length, width and depth values after divid-

ing all values by length (Thompson et al. 1993). The value

for spherical seeds was zero and increased to 0.3 when the

shape became flatter or elongated. The measurements of

seed size and shape included appendages, to understand

natural seed dispersal.

Seedmovement experiment to investigate secondary

seed dispersal

Secondary seed dispersal including burial was experi-

mentally quantified in the three investigated succes-

sional stages, i.e. on bare ground and in R. alba and

M. japonica grasslands. The seeds of R. alba, M. japonica

and L. sessilifolia were painted red using a small amount

of lacquer, and those of D. rotundifoliawere marked with

a white felt-tip marker. Four 10 cm 9 10 cm plots (one

plot per species) constituted one block, and 20 blocks

were established at 1-m intervals in each successional

stage. Therefore, a total of 80 plots were established in

each of the three successional stages. The litter thickness

in each plot was measured using a ruler at the beginning

and the end of the experiment. On 3 Oct 2010, soon

after primary seed dispersal ceased, marked seeds of each

species were dispersed from above the peat on bare

ground or on top of the litter in the R. alba andM. japon-

ica grasslands. For each species, there were 20 plots in

each stage, and 100 marked seeds of a single species

were dispersed in each plot. To investigate the effects of

snowmelt water on seed movements, the seeds were

retrieved from half of the plots on 5 Nov 2010, prior to

snow accumulation, and from the remaining plots on 20

Apr 2011, soon after snowmelt. During each retrieval

time, ten plots per species were randomly selected and

sampled for each of the three stages. First, we counted

the number of seeds remaining on the bare peat surface

or within the litter in the selected plots and removed

them. Then, we investigated the movement of seeds into

the peat by collecting peat layers and counting the seeds


C. Egawa & S. Tsuyuzaki Litter accumulation controls seed bank formation

within the peat. The peat was divided into two layers,

0–2- and 2–4-cm deep, and each peat layer was collected

separately. Therefore, we obtained two peat layers per

plot. The number of marked seeds in each peat layer was

counted under a binocular stereomicroscope. No

marked seeds had germinated at either retrieval time

because the seeds require several weeks after snowmelt

for germination to occur in the post-mined peatland

(Egawa & Tsuyuzaki 2011).

Seed burial experiment to quantify the availability of

viable seeds in litter and peat

To form a seed bank, seeds should remain viable and un-

germinated for a certain period of time. We examined

what proportion of dispersed seeds retained viability and

had the potential to form a seed bank through a seed burial

experiment conducted at various depths. Prior to burial,

the seeds were cold-stratified on moistened filter papers

(Whatman #1) in Petri dishes (9-cm diameter) for 1 mo at

2 °C in the dark. Soon after cold stratification, the seeds

were packed into capped transparent plastic tubes 23 mm

in height and 13 mm in diameter for the seed burial exper-

iment. Four holes, 1 mm in diameter, were drilled on the

side of each tube to maintain moisture (Tsuyuzaki 2006).

Each tube contained 20 cold-stratified seeds of one of the

four species and washed sea sand (20–35-mm mesh;

Wako, Osaka, JP). On 27 May 2010, just before seed ger-

mination commenced in the field, the tubes were buried at

the peat surface (0 cm) and at a depth of 4 cm (4 cm)

under the bare ground. In the R. alba and M. japonica

grasslands, the tubes were buried within the litter (hereaf-

ter, litter), in addition to the 0- and 4-cm peat layers. For

each of the successional stages, ten tubes per layer per spe-

cies were buried at 1-m intervals along two 4-m transects

established close to the plots used in the seed movement

experiment. We measured the litter thickness where the

tubes were buried. After the seeds had experienced a suit-

able germination period twice (spring 2010 and 2011), all

seeds were retrieved on 8 Jul 2011. We counted the num-

ber of seeds germinated inside the tubes, then checked the

viability of the remaining seeds through germination tests

and embryo cutting tests. The germination tests were con-

ducted with ten replicates of 50 seeds placed on moistened

filter papers in Petri dishes. The dishes were placed in an

incubator at 5 °C/25 °C (12 hr/12 hr) under 12 hr of

white fluorescent light (23 lmol�m�2�s�1).When seed ger-

mination was not recorded after more than 1 mo, the via-

bility of ungerminated seeds was examined by cutting the

embryos with a razor. The proportion of viable seeds able

to form a seed bank was calculated from the sum of the

number of germinated seeds detected in the germination

test and the ungerminated, but viable seeds detected in the

embryo-cutting test. Seed predation was prevented by the

plastic tubes and was not considered in the analysis. Addi-

tionally, predation appears to be weak in the post-mined

peatland (Egawa & Tsuyuzaki 2011).

The light and temperature at the peat surface and at a

depth of 4 cm were measured at 1-hr intervals from 28

May 2010 to 7 Jul 2011 using light/temperature sensors

(HOBO UA-002-64, Onset, MA, US) for each successional

stage. The light and temperature within the litter were also

measured in the R. alba and M. japonica grasslands. To

investigate the relative influence of litter and standing veg-

etation on the light and temperature, the removal of litter

and vegetation was conducted on 5 Jul 2011 in the R. alba

and M. japonica grasslands. We established a 50 cm 9

50 cm plot for each of three treatments, i.e. litter removal,

vegetation removal and control where litter and vegetation

remained intact, in each grassland. Litter was removed

using a rake and vegetation was cut at 5-cm height. The

light and temperature at the peat surface on each plot were

measured at 1-hr intervals from 6 Jul to 13 Oct 2011 using

the light/temperature sensors described above. Photosyn-

thetically active radiation (PAR) was calibrated through a

comparison between the light/temperature sensor and a

PAR sensor (S-LIA-M003, Onset) established on the bare

ground. In the study site, the mean water content of peat

from the surface to a 12-cm depth from May to August

was more than 70% for all three successional stages

(Egawa & Tsuyuzaki 2011).

Statistical analysis

We employed a correlation model approach to quantita-

tively investigate how litter thickness affects secondary

seed dispersal and the availability of viable seeds across the

three successional stages. Specifically, we developed statis-

tical models describing the quantitative relationships

between litter thickness and the probability of seed move-

ment and maintenance of viability. This analysis allowed

us to directly examine the effects of litter accumulation on

the fate of the seeds.

Seed movement model

At each retrieval, we categorized the movement of seeds

into the following four groups: (1) seeds emigrating out-

side of the plot in which the seeds were dispersed (N1); (2)

seeds remaining at their initial location, i.e. on the peat

surface on the bare ground and within the litter layer in

the two grasslands (N2); (3) seeds reaching a depth of 0–

2 cm (N3); and (4) seeds reaching a depth of 2–4 cm (N4).

We obtained the values N2, N3 and N4 by counting the

seeds in the retrieved samples as described above. Then we

calculated N1 as 100 – (N2 + N3 + N4), where the value



100 represents the number of seeds dispersed in each plot.

Therefore, N1 might include the number of seeds removed

by insects or animals. We assumed that the dispersed seeds

would exhibit one of the four types of movement with a

probability of q: q1 is the probability of the seeds emigrat-

ing from their initial locations; q2 is the probability of the

seeds remaining at their initial locations; and q3 and q4are the probabilities of the seeds shifting to the shallow

(0–2 cm) and deep (2–4 cm) peat layers, respectively.

We analysed how the litter thickness and snowmelt

water affected these probabilities for each species via

generalized linear mixed models (GLMM) in which the

litter thickness, retrieval season (Nov 2010 and April

2011) and their interaction were included as fixed fac-

tors, and the replicate plots were included as a random

factor. We applied a logit-link function with binomial

errors because the responsible variable was proportional

(Crawley 2005; Galeti et al. 2006). The probability dis-

tribution can be described as follows:

Prob ðNn j 100; qnÞ ¼ 100

Nn

� �q100n ð1� qnÞ100�Nn

and the probability of seed movement, qn, is a function of

the linear predictor Z, as follows:

qn ¼ 1

1þ expð�ZnÞ

and Zn ¼ b0n þ b1n � Litterþ b2n � Seasonþ b3n� ðLitter� SeasonÞ þ rn

where n indicates the seed movement categories from 1

to 4. Litter and Season indicate the litter thickness in

each plot and retrieval season, respectively. b0n is the

intercept, and b1n, b2n and b3n are the regression coeffi-

cients. rn is a random effect on the plots. To select the

best models, step-wise model selection based on Ak-

aike’s information criterion (AIC) was conducted (Burn-

ham & Anderson 2002).

Seed viability model

The quantitative effects of the litter thickness and burial

depth (litter, 0 cm or 4 cm) on the probability that the

seeds retained viability for 1 yr were analysed for each spe-

cies using GLMM inwhich the litter thickness, burial depth

and their interaction were included as fixed factors and the

replicate burial points as a random factor. The number of

viable seeds, N, was assumed to follow the binomial errors

(Crawley 2005), such that N ~ Bin (20, P), where 20 is the

number of seeds in a tube, and P represents the probability

that the seeds retained viability for 1 yr for each species. In

this analysis, P is described as a logit-link function using

the linear predictor Z as follows:

P ¼ 1

1þ expð�ZÞ

Here, the linear predictor Z is

Z ¼ b0 þ b1 � Litterþ b2 � Burial depthþ b3 � ðLitter� Burial depthÞ þ r

where b0 is the intercept; b1, b2 and b3 are the regression

coefficients; and r represents the random effect of burial

points. The best models were selected based on the AIC

(Burnham & Anderson 2002). All statistical analyses were

conducted using the R (v. 2.12.1) statistical environment

(R Core Development Team, Vienna, AT).

Results

Environmental changes associatedwith litter

accumulation through succession

Litter thickness increased with the progress of succession.

Litter was absent on bare ground, whereas 2- to 5-cm thick

(mean = 4 cm) litter accumulated on the R. alba grass-

land, and 6- to 15-cm thick (9 cm) litter accumulated on

the M. japonica grassland. The litter quality was dependent

on the dominant species of the two grasslands: the litter in

the R. alba grassland was mostly composed of leaves and

culms of R. alba, while that in the M. japonica grassland

consisted ofM. japonica leaves.

The PAR and daily temperature fluctuations, i.e. the

difference between the daily maximum and minimum

temperatures, decreased with the progress of succession.

The PAR was considerably higher on bare ground than on

the peat surface covered with litter in the R. alba and

M. japonica grasslands throughout the germination season

(Table 1). The PAR in the litter layers varied with litter

thickness: the PAR from May to July in the M. japonica

grasslandwhere the litter thickness was 9 cmwas less than

half of that in the R. alba grassland where the litter thick-

ness was 4 cm. The PAR at a depth of 4 cm was zero in all

successional stages.

On the other hand, daily temperature fluctuations at

the 4-cm depth decreased with the progress of succes-

sion (Table 1). The daily temperature fluctuations at this

depth from April and July were 3.5–5.8 °C on bare

ground, 2.1–3.2 °C in the R. alba grassland, and 1.1–

1.6 °C in the M. japonica grassland. The progress of suc-

cession also affected the daily temperature fluctuations

at the peat surface during the same period, which ranged

from 17.3–31.2 °C on bare ground, 4.0–7.1 °C in the

R. alba grassland, and 3.3–5.3 °C in the M. japonica

grassland.

The PAR and temperature at the peat surface were

affected more by litter removal than by vegetation



removal. In the M. japonica grassland, the daily mean PAR

at the peat surface in July 2011 was 20 lmol�m�2�s�1 in

the control plot where litter and vegetation remained

intact, 44 lmol�m�2�s�1 in the vegetation removal plot

and 199 lmol�m�2�s�1 in the litter removal plot. As well as

the M. japonica grassland, the PAR was higher in the litter

removal plot (325 lmol�m�2�s�1) than in vegetation

removal plot (200 lmol�m�2�s�1) in the R. alba grassland

(73 lmol�m�2�s�1 in the control). The daily mean temper-

ature in the same period was 19.7 °C (M. japonica grass-

land) and 20.9 °C (R. alba grassland) in the control, 20.5

and 22.2 °C in the vegetation removal plot and 21.2 and

23.4 °C in the litter removal plot. These results indicate

that the differences in PAR and temperature among suc-

cessional stages were related to both litter and standing

vegetation, and the effect of litter was higher than that of

vegetation.

Seed size and the patterns of secondary seed dispersal

The four study species differed in the sizes and shapes of

their seeds (Table 2). The seed size was smallest in D. ro-

tundifolia, followed by L. sessilifolia, R. alba and finally

M. japonica, which produced the largest seeds. D. rotundifo-

lia seeds were winged, the seeds of L. sessilifolia had a

smooth surface, while the seeds of R. alba had a beak on

top and hairs at the base, and the M. japonica seeds had

lemmas. The variance in seed dimensions was smallest

in L. sessilifolia, followed by R. alba, M. japonica and

D. rotundifolia, indicating that L. sessilifolia had the round-

est-shaped seeds, and D. rotundifolia had the most elon-

gated seeds among the four species.

The proportions of seeds that emigrated, were retained

and were buried differed among species with different-

sized seeds (Fig. 1). The best model selected via GLMM

analysis showed that the litter thickness significantly

affected the probability of seed movement for all species

(Fig. 1; Appendix S1). Overall, seed emigration from the

initial location decreased, while seed retention increased

with increases in litter thickness. The smallest seeds, pro-

duced by D. rotundifolia, had mostly emigrated from the

surface of the bare ground prior to the snowy season. For

the other three species, the probability of emigration on

bare ground in April was even higher than in November,

indicating that snowmelt water promoted seed emigration.

Because most of the seeds emigrated, the proportion of

buried seeds was nearly zero on the bare ground for all spe-

cies: few seeds were found at depths of 0–2 and 2–4 cm

under bare ground.

As litter accumulated through the progress of succes-

sion, the probability of seed retention increased, and the

probability was higher in November than in April for

all species. For D. rotundifolia and L. sessilifolia seeds, theTable

1.Dailymean

photosynthetically

active

radiation(PAR)andtemperature

from

ApriltoJulyof2010and2011at

variousdepthsinthreesuccessionalstages(bareground,R

.albagrasslandandM.japon-

icagrassland).Maxim

um

andminim

um

valuesarealso

showninparenthesesfortemperature,asaremaxim

um

valuesforPAR.Theminim

um

valuesofPARwere

0lm

ol�m

�2�s�

1atalldepthsdueto

midnight

darkness.M

easurementswere

perform

edat

threedepths:insidelitter,peat

at0cm

andpeat

at4cm

belowthegroundsurface.

BareGround

R.albaGrassland

M.japonicaGrassland

Peat

0cm

Peat

4cm

Litter

Peat

0cm

Peat

4cm

Litter

Peat

0cm

Peat

4cm

PAR(lmol�m

�2�s�

1)

April

–0(0)

77.0(389.2)

10.0(12.6)

0(0)

49.4(332.1)

8.5(14.8)

0(0)

May

601.6(1657.2)

0(0)

136.0(661.2)

11.6(28.3)

0(0)

53.5(352.7)

9.6(17.8)

0(0)

June

428.7(1389.0)

0(0)

152.6(680.3)

13.4(47.8)

0(0)

41.4(253.6)

8.6(14.2)

0(0)

July

333.5(1167.3)

0(0)

98.7(429.1)

10.1(23.6)

0(0)

25.1(102.5)

7.6(9.6)

0(0)

Temperature

(°C)

April

–4.1(6.0,2.5)

4.1(8.6,1.0)

3.8(6.1,2.1)

3.8(4.9,2.8)

3.9(8.5,1.1)

3.0(4.8,1.5)

3.0(3.6,2.5)

May

14.3(31.3,0.1)

8.2(11.2,5.5)

8.8(16.7,2.9)

9.0(12.7,6.0)

7.9(9.6,6.4)

7.4(14.0,2.7)

6.1(8.8,3.5)

5.8(6.6,5.0)

June

18.8(30.5,11.6)

16.6(19.7,13.9)

17.3(26.5,12.1)

15.7(20.0,12.9)

15.0(16.7,13.6)

14.6(21.2,10.4)

12.6(14.9,10.7)

10.9(11.5,10.3)

July

22.0(33.1,15.8)

20.8(23.7,18.6)

21.1(28.1,17.0)

20.1(23.7,17.8)

19.7(21.2,18.5)

18.2(22.6,15.1)

16.7(18.1,15.5)

14.5(15.1,14.0)

–:Datanotavailable.



Table 2. Seed mass (mean � SD), variance of seed dimensions, primary dispersal type and seed bank persistence in the post-mined peatland for the four

study species. The primary dispersal type and seed bank persistence follow Egawa et al. (2009). The seed mass and seed dimensions (length, width and

depth) were measured for 50 seeds per species after being air-dried for 1 wk in paper bags at room temperature. The seeds included appendages.

SeedMass (mg) Variance of

Seed Dimensions

Primary Dispersal

Type

Seed Bank

Persistence

Drosera rotundifolia 0.01 � 0.003 0.176 Wind Persistent

Lobelia sessilifolia 0.25 � 0.04 0.097 Gravity/Wind Unknown

Rhynchospora alba 0.87 � 0.13 0.113 Gravity Transient

Moliniopsis japonica 1.82 � 0.40 0.150 Gravity Transient

(b)

(a)

(c)

(d)

Fig. 1. Relationships between litter thickness and the proportions of four categories of seed movement: (a) emigration, (b) retention at the initial

location, (c) 0–2 cm burial in peat, and (d) 2–4 cm burial in peat, for the four species. Dashed and solid lines show the estimated probabilities of

seed movement in Nov 2010 and April 2011 in the best models (GLMM). The selected fixed parameters in the models are also shown. When the

retrieval season was not selected as a parameter in the models, the lines of the two seasons overlap. NS indicates that no parameters were

selected in the best models. Different symbols represent differences in the successional stages: triangles (▲,M) = bare ground; squares

(&,h) = R. alba grassland; circles (●,s) = M. japonica grassland.



difference in the the probability of retention between the

two seasons became higher with an increase in litter thick-

ness. In contrast, it became lower for the two other species,

particularly for M. japonica. These findings indicate that

thicker litter retained larger seeds for a longer period. The

small seeds of D. rotundifolia and L. sessilifolia did not

remain within the thick litter for long but emigrated or

moved downward. The probability of seeds travelling to

the shallow (0–2 cm) peat layer was higher under thicker

litter for D. rotundifolia, L. sessilifolia and R. alba. In addi-

tion, as litter accumulated, the probability became higher

in April than in November for D. rotundifolia and R. alba.

These results indicate that the seeds of the three species

trapped by thick litter passed through the litter layer and

travelled down to the peat, and snowmelt water was likely

to promote these downward movements. Although the

seeds of R. albawere the second largest among the studied

species, their downward movements were more similar to

those of the two small-seeded species than to M. japonica,

which produced the largest seeds. Only a few seeds of

M. japonica were found in the 0–2 cm peat layer, irrespec-

tive of litter thickness. Therefore, M. japonica seeds rarely

moved once they were trapped within the litter. The pro-

portion of seeds reached depths of 2–4 cm was nearly zero

for all species, even when thick litter accumulated.

Availability of viable seeds after being buried at various

depths

The best model based on the GLMM analysis showed that

the probability that seeds retained viability for 1 yr (here-

after, the probability of seed viability) was positively corre-

lated with the litter thickness and burial depth for all

species (Fig. 2; Appendix S2). The proportion of viable

seeds was larger, while that of germinated seeds was smal-

ler under thicker litter andwith deeper burial for all species

(Table 3). For D. rotundifolia and R. alba, the proportion of

decayed seeds decreased with an increasing burial depth.

At the peat surface on the bare ground,most of the seeds

of all of the species germinated in the tubes during the

experiment, and the proportion of remaining viable seeds

was less than 5%. Similarly, a large proportion of seeds

germinated within the thin litter in the R. alba grassland.

The probability of seed viability on the peat surface was

higher under thicker litter for all species (Fig. 2), most

likely because the micro-environment under thick litter

maintained the seeds ungerminated in the tubes.M. japon-

ica, which produced the largest seeds, exhibited a linear

increase in the probability of seed viability on the peat sur-

face with an increase in litter thickness, whereas that of

the other three species was sigmoidal. The probability of

seed viability at the depth of 4 cm was also higher under

thicker litter for all species, particularly forM. japonica. The

proportion of viable M. japonica seeds the depth of 4 cm

was lowest on the bare ground (19%) with no litter; the

proportion increased with an increasing litter thickness to

52% in the R. alba grassland and 60% in the M. japonica

grassland. In contrast, the proportion of germinated

M. japonica seeds at the depth of 4 cm was highest under

bare ground and lowest in theM. japonica grassland. These

results indicate that the litter contributed to maintaining

the seeds ofM. japonica ungerminated, not only at the peat

surface but also in the deep peat layer. The proportion of

viable seeds of R. alba at the 4-cm depth in the peat also

increased with increasing litter thickness, but the increase

was lower than that observed forM. japonica.

Discussion

Effects of litter on secondary seed dispersal

Our seed movement experiment showed that litter accu-

mulation through succession greatly altered secondary

Fig. 2. Relationships between litter thickness and the proportion of viable seeds after being buried at three different burial depths (litter, 0 and 4 cm) for

the four species. Solid grey, dashed and solid black lines show the probability of seeds retaining viability for 1 yr within the litter, at the peat surface

(0 cm) and at a depth of 4 cm (4 cm), respectively, estimated in the best models (GLMM). The best models for all species include litter thickness, burial

depth and their interaction as fixed parameters. Different symbols indicate differences in the successional stages: triangles (▲,M) = bare ground,

squares (&,&,h) = Rhynchospora alba grassland, circles (●,●,s) = Moliniopsis japonica grassland.



seed dispersal patterns. In the study sites, the lack of litter

at the earliest stage of succession, i.e. the bare ground

stage, promoted the emigration of seeds after landing on

the ground. In addition, the probability of emigration was

higher in April than in November. This was most likely

because the sheet flow of snowmelt water on bare ground

transported a large number of seeds. On the flat ground

surface, seeds can be dispersed broadly bywind and rainfall

(Greene & Johnson 1997; Emmerson et al. 2010). Because

there are no physical barriers to the peat surface in bare

ground study sites (Koyama & Tsuyuzaki 2010), direct

wind and rainfall contribute to the emigration of seeds. As

a result of dispersal to a wide area by such physical agents,

seeds often become lodged in depressions or caught in veg-

etation or debris in distant areas (Emmerson et al. 2010).

Thus, some part of the emigrated seeds from the bare

ground sites might have been captured in litter and/or veg-

etation in adjacent sites in the post-mined peatland. The

seeds emigrating from the bare ground surface might ger-

minate and establish seedlings or form a seed bank in a dis-

tant site.

As litter accumulated through the progress of succes-

sion, seed emigration decreased, and seed retention

increased. Small seeds passed through the litter layer and

reached the peat surface, whereas large seeds were more

likely to remain within the litter even after they were

exposed to snowmelt water. These results agree with those

of Rotundo & Aguiar (2005) and Ruprecht & Szab�o (2012),

who showed that litter selectively traps large seeds more

than small seeds. This sieve effect is largely determined by

the shape of the plant parts that constitute the litter. For

instance, the broad-leaved litter of bracken ferns acts as a

physical barrier to reaching the soil surface, even for small

and light seeds, and seeds within this type of litter are unli-

kely to move into the soil layer (Ghorbani et al. 2006). In

contrast, litter composed of narrow-leaved grasses allows

seeds to shift after seed trapping occurs (Ruprecht & Szab�o

2012). Similarly, the grass litter originating frommonocot-

yledon species in our study sites may selectively alter sec-

ondary dispersal patterns depending on seed size.

We focused primarily on the effects of seed size on sec-

ondary seed dispersal in the present study. In addition,

seed shape and appendages may affect the patterns of seed

movements (Chambers et al. 1991; Thompson et al.

1993). These seed characteristics may account for at least

a part of the difference in dispersal patterns between spe-

cies that produce seeds of similar sizes. For instance, the

retention probability for R. alba seeds on the bare ground

was higher than that for M. japonica seeds, even though

M. japonica seeds are larger than R. alba seeds. This may

be because R. alba seeds develop seed coat hairs, whereas

M. japonica seeds lack such appendages. Similarly, the

roundest-shaped seeds of L. sessilifolia were more likely toTable

3.Mean

proportionsofviab

le,germ

inatedanddecayedseedsafter1yr

ofburialat

variousdepthsinthreesuccessionalstages(bareground,R

.albagrasslandandM.japonicagrassland).Thegerm

i-

nationratesafterburialarealso

showninparentheseswhenungerm

inatedseedswere

includedintheviab

leseeds.Litter,peat

0cm

andpeat

4cm

indicatesampleswithinlitter,at

thepeat

surface,andat

the4-cm

depth

inpeat,respectively.

Drosera

rotundifolia

Lobelia

sessilifolia

Rhynchospora

alba

Moliniopsisjaponica

Viable(%)

Germ

inated(%)

Decayed(%)

Viable(%)

Germ

inated(%)

Decayed(%)

Viable(%)

Germ

inated(%)

Decayed(%)

Viable(%)

Germ

inated(%)

Decayed(%)

After1yr

ofburialin

BareGround

Peat

0cm

1.4

77.9

20.7

0.0

100.0

0.0

1.9(0.6)

58.1

40.0

4.4(0.0)

95.6

0.0

Peat

4cm

82.3

3.8

13.9

92.8

5.6

1.6

60.7(60.1)

14.4

24.9

19.4(12.5)

73.1

7.5

R.albagrassland

Litter

0.0

63.5

36.5

0.0

100.0

0.0

1.7(0.6)

78.3

20.0

4.0(3.5)

94.0

2.0

Peat

0cm

55.5

29.5

15.0

17.8(17.0)

82.0

0.0

36.0

37.0

27.0

15.5(12.0)

79.0

5.5

Peat

4cm

95.5

3.0

1.5

87.0(86.5)

12.5

0.5

88.1

3.0

8.9

52.0(34.0)

40.0

8.0

M.japonicagrassland

Litter

24.5

62.0

13.5

6.1

93.3

0.6

22.0(21.0)

57.0

21.0

7.1(3.6)

92.9

0.0

Peat

0cm

76.0

17.0

7.0

93.7

5.0

1.3

72.5(71.5)

1.5

26.0

41.1(23.3)

58.3

0.6

Peat

4cm

93.7

3.0

3.3

97.1(96.6)

1.5

1.4

88.9(88.9)

0.5

10.6

59.5(52.0)

34.5

6.0



move downward to the peat surface than the elongated

seeds of D. rotundifolia, despite the fact that the seeds of

the latter species are much smaller than those of the for-

mer. A detailed investigation is needed to clarify the influ-

ence of seed shape and appendages on secondary seed

dispersal.

Effects of litter on viable seeds in the seed bank

Our experiment showed that litter accumulation could

alter the input of viable seeds to the seed bank by suppress-

ing seed germination, which is an important process that

reduces the seed density in the seed bank (Hyatt & Casper

2000). We found that litter affected light and daily temper-

ature fluctuations, both of which are known to be key ger-

mination cues (Saatkamp et al. 2011). First, the reduced

light intensity within or below litter layers can suppress

seed germination, thereby increasing the number of seeds

potentially contributing to seed bank formation. In this

study, the four species appeared to differ with respect to

their germination cues. At a depth of 4 cm, where light is

not available, the proportion of germinated M. japonica

seeds was considerably higher (35–73%) compared to the

other three species (0.5–14%), suggesting that the latter

three species may require light for germination. Because

light intensity decreased with the thickness of litter, the

accumulation of litter may facilitate the formation of a per-

sistent seed bank for species that require light for germina-

tion. Second, a thick litter layer contributed to reducing

the daily temperature fluctuations, even in deep peat, i.e.

at a 4-cm depth, and the small temperature fluctuations

beneath thick litter might retain seeds in an ungerminated

and viable state in the deep peat layer. As litter accumula-

tion alters the light intensity and daily temperature fluctu-

ations simultaneously, the relative influence of the two

factors on seed germination and seed viability in each spe-

cies needs to be examined by manipulating these factors

independently. Standing vegetation interacts with litter to

affect the microclimates both on and under the ground.

The biomass of vegetation generally increases with the

progress of succession (Bazzaz 1996), and this process may

also contribute to increasing the number of viable seeds in

the seed bank.

For all species, the proportion of viable seeds was higher

when they were buried at deeper depths. Deeper burial

reduced not only the proportion of germinated seeds but

also that of decayed seeds, particularly for D. rotundifolia

and R. alba. We did not determine the reasons for seed

decay during burial. We hypothesize that attack by patho-

gens is a possible reason, as it is known that pathogen

activity becomes lower in deep soil (Dalling et al. 1998). A

further study is needed to investigate the effects of patho-

gens on seed bank depletion in the study site.

Seed germination causes loss of viable seeds in the seed

bank, but it can also contribute to population growth.

Although we did not investigate the success of the estab-

lishment of germinated seeds, it is expected to depend on

the habitat preference of each species. A previous study in

the post-mined peatland showed that the earliest colo-

nizer, R. alba, successfully established seedlings on bare

ground, while the later colonizer M. japonica failed to

establish seedlings (Egawa & Tsuyuzaki 2011). Similarly,

D. rotundifolia was not observed in the M. japonica grass-

land, even though its seeds were found (Egawa et al.

2009), indicating that this species could not establish seed-

lings there.

Seed bank formation through succession

The results of this study suggest that seed bank formation

processes change with time for both small and large seeds

because secondary seed dispersal and the availability of

viable seeds at various depths varied with litter accumula-

tion through succession. Although the number of viable

seeds of the four study species was larger when the seeds

were experimentally buried at a deeper depth, the vertical

movement of seeds was restricted to the litter and the shal-

low peat layer, less than 2-cm deep, at least within the

investigated experimental period. However, shallow burial

of seeds is effective to maintain seeds in an ungerminated

state, as shown in this study and in others (Bonis & Lepart

1994; Benvenuti et al. 2001). Therefore, we propose that

shallow burial of seeds that pass through litter is an impor-

tant process for seed bank formation and, consequently,

for population dynamics. It is possible that seeds become

buried at a depth of more than 2 cm after a period longer

than that of the experiment conducted here. Deeply buried

seeds can form a persistent seed bank and may play a role

in population stability.

Our results show that most of the experimental seeds

emigrated from the bare peat surface. Moreover, the num-

ber of seeds primarily dispersed on bare ground might be

smaller than that in vegetated sites in the post-mined peat-

land because bare ground lacks mother plants, and coloni-

zation depends on incoming seeds from adjacent sites.

Even if some proportion of the seeds remains at the surface

on bare ground, most of the seeds will germinate within a

year, as shown by the seed burial experiment. Thus, the

formation of a seed bank of the studied species in areas of

bare ground is expected to proceed very slowly or may be

restricted until litter accumulates. In fact, Egawa et al.

(2009) showed that the seed bank density in bare ground

in the post-mined peatland is much smaller than that in

vegetated areas with litter. As vegetation develops during

succession, the number of seeds produced and primarily

dispersed at a site generally increases (Walker & del Moral



2003). The present study showed that litter accumulation

through succession promoted seed retention at the investi-

gated sites and increased the number of viable seeds that

potentially form the seed bank. These results could explain

why seed bank formation often follows the development

of standing vegetation associated with litter during succes-

sion (Bekker et al. 2000; Walker & del Moral 2003). Fur-

thermore, we showed that small seeds were more likely to

pass through litter, and this secondary dispersal would pro-

mote the formation of a persistent seed bank at the peat

surface, while large seeds were likely to develop a transient

seed bank within the litter layer that accumulated with

developed vegetation. In fact, the small seeds of D. rotundi-

foliawere found more frequently in peat than in litter, and

the large seeds of M. japonica were concentrated more in

litter than in peat throughout the year in the vegetated

habitats, where thick litter accumulated in the post-mined

peatland (Egawa et al. 2009).

Litter accumulation is generally expected to increase the

relative success of large-seeded species in standing vegeta-

tion because seedlings produced from large seeds are more

likely to penetrate litter and become established under

shaded conditions compared to those from small seeds

(Xiong et al. 2001; Donath & Eckstein 2010). Therefore,

late-successional species that regenerate under dense vege-

tation and litter tend to produce larger seeds than early-

successional species (Jensen & Gutekunst 2003). Our study

suggests, however, that small-seeded species could remain

in the late-successional community due to forming a per-

sistent seed bank under a thick litter layer, even when

seedlings of these species fail to become established in

standing vegetation. The seed bank on the ground surface

covered by litter can contribute to the regeneration of

small-seeded species when litter is partly removed through

small disturbances, such as wind (Facelli & Pickett 1991).

Thus, the temporary dynamic processes of litter accumula-

tion and loss through succession may have long-term

effects on the dynamics of plant populations and the whole

community by determining the spatial distribution of the

seed bank.

Acknowledgements

We thank Y. Hoyo for her substantial assistance in our

fieldwork, and T. Kawagoe and anonymous reviewers for

fruitful comments, which helped to improve the manu-

script. We appreciate the support of R. Miyata and mem-

bers of the Plant Ecology Laboratory in Hokkaido

University. We are grateful to the staff of the Ministry of

the Environment of Japan and Toyotomi Town Office for

permission and support for this research. This work is

partly supported by grants from the Japan Society for the

Promotion of Science.

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Supporting information

Additional Supporting Information may be found in the

online version of this article:

Appendix S1. Statistical results of the best models

(GLMM) examining the relationships between litter thick-

ness and the probability of seed movement.

Appendix S2. Statistical results of the best models

(GLMM) examining the relationships between litter thick-

ness and the probability of seed viability.



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