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(American Journal of Botany. 2001;88:1813-1817.)
© 2001 Botanical Society of America, Inc.

Ecology

Persistence of seed bank under thick volcanic deposits twenty years after eruptions of Mount Usu, Hokkaido Island, Japan1

Shiro Tsuyuzaki2 and Masaki Goto

Graduate School of Environmental Earth Science, Hokkaido University, Sapporo 060-0810 Japan

Received for publication September 14, 2000. Accepted for publication March 8, 2001.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 STUDY AREA AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The topsoil that contained the seed bank became buried under thick tephra after the eruptions of Mount Usu during 1977 and 1978. To determine the seed bank potential of the topsoil 20 yr after the eruptions, i.e., in 1998, 408 100-cm3 samples were excavated under 115–185 cm of volcanic deposits. The topsoil was collected at 10-cm intervals along the horizontal scale and was divided into a 0–5 cm deep upper layer and a 5–10 cm deep lower layer. The seed bank was estimated by both the germination (GM) and flotation (FM) methods. In total, 23 species with an average seed density of 1317 seeds/m2 were identified by GM, and 30 species with a density of 2986 seeds/m2 were extracted by FM. The dominant species was Rumex obtusifolius, and perennial herbs, such as Carex oxyandra, Viola grypoceras, and Poa pratensis, were common. For nine species this study provided the first records for field seed longevity >20 yr. The seed density in the upper layer was double that in the lower layer, and the horizontal distribution was heterogeneous even at 10-cm intervals. We concluded that the seed bank has retained the original structure of the seed bank under the tephra and will persist longer with soil water content between 20 and 40%, no light, and low temperature fluctuations (±0.17°C of standard deviation in a day).

Key Words: buried seed populations • former topsoil • long seed longevity • Mount Usu • seed bank


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
STUDY AREA AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Seed longevity in nature is an important determinant of plant community dynamics because the wide range of seed dormancy strategies has evolved to adapt to various environmental changes and to maintain populations (Thompson and Grime, 1979 ). Furthermore, species with longer lived seeds have lower local extinction rates (Stöcklin and Fischer, 1999 ). There have been numerous studies conducted to detect seed longevity using experimental seed burial tests (Leck, Parker, and Simpson, 1989 ; Baskin and Baskin, 1998 ). Many seed longevity experiments have been conducted under somewhat unnatural conditions. For example, seeds collected from fields and placed into milk bottles for 100 yr would experience altered soil moisture and related factors when buried and periodically tested (Kivilaan and Bandruski, 1981 ). Evaluation of seed banks buried under natural conditions, e.g., volcanic ash, would provide more realistic data (Whittaker, Partomihardjo, and Riswan, 1995 ).

The seed bank buried under thick volcanic deposits persisted for 10 yr after the 1977–1978 eruptions on Mount Usu, northern Japan (Tsuyuzaki, 1991 ). This seed bank had been conserved because predators were few, the movements of seeds by erosion and animal carriers rare, and contamination from the vegetation did not occur due to thick volcanic deposits. Therefore, this seed bank provides a chance for the long-term monitoring of buried seed populations under natural conditions, and this paper reports the seed bank status 20 yr after the burial.


   STUDY AREA AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 STUDY AREA AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Mount Usu is located on Hokkaido Island (42°32' N, 140°50' E, 727 m in altitude in 1978) and is one of the most active volcanoes in Japan. The volcano is composed of two peaks, O-Usu (727 m) and Ko-Usu (609 m), enclosed by a caldera rim and crater basin. Before the 1977–1978 eruptions, the vegetation was dominated by broad-leaved forests consisting mostly of Populus maximowiczii and Betula platyphylla var. japonica and artificial meadows represented by Dactylis glomerata and Trifolium repens (Hara, 1978 ). Due to the thick volcanic ash deposits in 1977–1978, vegetation was completely destroyed on the summit area. Soon after the eruptions, vegetation recovery began as the result of vegetative reproduction, seeds in the former topsoil, seed immigration, and artificial seeding (Tsuyuzaki, 1987 ). Observations showed that seedlings of specific species were conspicuous in the gully where the former topsoil was exposed but did not appear in areas without the former topsoil (Tsuyuzaki, 1989 ). These seedlings apparently originated from the seed bank present in the former topsoil. Ten yeas after the eruptions, soil blocks were collected from the former topsoil that was buried 65–140 cm under the volcanic deposits. The seed bank consisted of at least 25 species of which seed density was ~2000 seeds/m2, and the dominant species was the nonnative Rumex obtusifolius (Tsuyuzaki, 1991 ).

In June 1998, we excavated four sites and collected 408 100-cm3 topsoil samples from the crater basin. To avoid the contamination of fresh seeds from the ground surface owing to the movements of volcanic deposits, gullies and adjacent areas were not selected for the excavations. Sites were resultingly 10–30 m from each other. When the ground surface of the former topsoil was reached, the thickness of volcanic deposits was measured. Dedpending on the conditions of volcanic deposits, the sizes of quadrats were determined as 40 x 40 cm (two quadrats) or 50 x 50 cm (two quadrats). The quadrat was divided into 10 x 10 cm subquadrats. Two soil samples were collected from the upper layer (0–5 cm deep) in each subquadrat, and then two soil samples were taken from the lower layer (5–10 cm). In each layer, the two samples were collected from upper-left and lower-right corners of each subquadrat to link upper and lower layers. One sample was used to test germination and another for the flotation test. Each soil sample was 20 cm2 in surface area and 5 cm in depth by a soil tin. Due to the collapse of one pit during the collection of soils in a 50 x 50 cm quadrat, we did not collect samples from the lower layer in one quadrat. Owing to this, we used the samples collected from both layers for the sum total of upper and lower layers. In each site, three 100-cm3 topsoil samples were also collected to measure water content.

To estimate the species composition and seed density, two methods were used: the germination method (GM) and the flotation method (FM). Nomenclature follows Ohwi and Kitagawa (1983) . The germination method was conducted in a greenhouse in the Faculty of Science, Hokkaido University, Sapporo, Japan, immediately after the soil collections. The soils were sprayed over vermiculite in a <1 cm thick layer (except for large volcanic particles contained therein) in a pot (25 x 20 cm in surface area, 10 cm in depth). The observations were continued for 5 mo until germination was no longer observed. After the species could be identified, the seedlings were clipped out. Seedlings that could not be identified were transplanted to another pot and grown until identification could be made.

For FM samples, we used a centrifuged flotation method following (Tsuyuzaki, 1994 ). The soil samples were agitated with 50% K2CO3 flotation solution (1.54 g/cm3). The mixture was centrifuged (~4000 g) for 4–5 min, and then nearly all organic debris floated. All organic debris was decanted and filtered with two layers of miracloth (Calbiochem, California). The seeds were rinsed with distilled water and kept in a refrigerator at 5°C until used. The seeds were identified by morphological traits using voucher seed collections. After the identification, the length, width, and thickness of seeds were measured using a binocular stereomicroscope. The seed volume was evaluated as if the shape were oval sphere. Any seeds that could not be identified by morphological traits were germinated in an incubator at 15°/25°C (12 h/12 h). The viability of seeds extracted by the flotation test was not estimated by tetrazolium tests because of overestimation due probably to the staining of bacteria and/or fungi (Tsuyuzaki, 1991 ). Instead, the viability was estimated from their firmness and intact appearance using a seed-crushing technique, i.e., the albumen of seeds crushed by a needle was not juicy and/or became brown; those seeds were considered to have died (Naka and Yoda, 1984 ; Tsuyuzaki, 1991 ).

To estimate the spatial heterogeneity of the seed bank, the vertical distribution of the number of seeds was estimated by Wilcoxon's binomial test after Bonferroni corrections (Zar, 1996 ). Coefficients of variation (CV) were calculated to investigate the spatial heterogeneity of seed density (Thompson, 1986 ). When CV is high, the distribution is contagious and heterogeneous. To determine the difference of detection sensitivity between GM and FM, Spearman's rank correlation coefficients were obtained on the total number of seeds and species.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 STUDY AREA AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
The thickness of volcanic deposits over seed bank sample sites ranged from 115 to 185 cm. The surface of the former topsoil was clearly defined, indicating that the surface of the former topsoil had not been disturbed. A few ant nests were established on the ground surface but were <50 cm deep. Visible animals were not observed in >50 cm deep volcanic deposits. Therefore, seeds produced by the present vegetation could not percolate into the former topsoil. Water content in the former topsoil ranged from 22.3% to 36.4%.

In total, 23 and 30 species were detected by GM and FM, respectively (Table 1). Twenty-two species were identified, of which six were nonnative. There were 1.31 ± 0.17 species/m2 by GM and 2.87 ± 0.36 species/m2 by FM in the 10 cm deep layer. Mean number of seeds or seedlings per sample was 2.13 ± 0.30 according to the GM and 8.25 ± 1.49 according to the FM. Densities of seedlings and seeds were estimated to be 1317 ± 469 individuals/m2 and 2986 ± 1996 individuals/m2 as determined by GM and FM, respectively. Spearman's rank correlation coefficients were +0.423 on number of seeds between GM and FM (significant at P < 0.01, N = 61) and +0.462 on number of species (P < 0.01). Therefore, the two methods were roughly comparable, although total number of seeds detected by FM was significantly higher than by GM. Rumex obtusifolius was dominant and accounted for >40% of the total number of individuals. Perennial herbs such as Carex oxyandra, Viola grypoceras, and Poa pratensis were common. Four annuals were germinated, but their density was very low, and only one woody species was detected. The habitat preferences of the species present showed a wide array of habitats: open forest (e.g., Betula spp. and Aralia cordata), grassland (Rumex obtusifolius and Poa pratensis), and wet sites (Ranunculus repens and Juncus effusus var. decipiens).


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  		Table 1. Seeds detected by germination and flotation methods. Values indicate mean seed density (no./m2) ± 1 SD. A few unidentified species might have been germinated using both methods

 
Using the FM, the vertical distribution showed that the upper layer contained more species and seeds (Table 1). Two species, Hypericum erectum and an unidentified species, were distributed only in the lower layer. The seed sizes ranged from 0.03 to 2.75 mm3 for all 30 species detected by FM. Hypericum erectum had the smallest seeds, and the unidentified species had the second smallest seeds. Species of which the seed volume was <0.15 mm3 represented 5.4% of the total seeds in the upper layer, while they accounted for 22.7% in the lower layer, indicating that smaller seeds tended to be distributed more in the lower layer. In contrast, species of which the seed volume was >1.05 mm3, i.e., three unidentified species, were detected in the upper layer only.

Horizontal distribution of total seeds showed high spatial heterogeneity (Fig. 1). The CV was 2.56 on GM and 16.5 on FM for total number of seeds, and CV of R. obtusifolius, the dominant species, showed 2.15 on GM and 7.05 on FM (Table 2), indicating that the spatial heterogeneity was very high and clump sizes were irregular. The CV in the upper layer was higher than in the lower layers.



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  		Fig. 1. Spatial distribution of the total number of seeds in a 50 x 50 x 10 cm quadrat of which density was the highest in the four quadrats surveyed. The sizes of circles indicate that number of seeds (flotation method) or seedlings (germination method) in each 10 x 10 cm subquadrat. The maximum circle indicates 52 seeds. The numeral within each box represents the number of species

 

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  		Table 2. Coefficients of variation (CV) on number of seeds buried in the former topsoil. N: number of samples

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 STUDY AREA AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
Because the site locations of the present survey were ~50 m distant from the survey sites used for the study 10 yr after the eruptions, an exact comparison is not possible. However, the dominant species was the same, i.e., Rumex obtusifolius, and the seed number and density did not differ greatly between 10 yr (Tsuyuzaki, 1991 ) and 20 yr after the eruptions (Table 1). Most seed banks have been shown to be heterogeneously distributed due to microtopography difference (Thompson, 1986 ; Bigwood and Inouye, 1988 ). More seeds were distributed in the upper layers of soil as shown in references in other studies (e.g., Kramer and Johnson, 1987 ), and thus CV is lower in the lower layers (Kellman, 1978 ). However, species that produced the smallest seeds were detected only in the lower layers, perhaps because smaller seeds are more easily moved to the lower layer (Fenner, 1985 ).

Requirements for seed germination include temperature, temperature fluctuation, light, etc. While seed germination for many species is enhanced by daily temperature fluctuations (Baskin and Baskin, 1998 ), the standard deviation of temperature fluctuation for a single day was <0.23°C under 50 cm of ash on Mount Usu (Tsuyuzaki, 1991 ). Also, the mean daily temperature was <15°C in August, and light could not penetrate to the former topsoil. Wet soil occasionally maintains seed germination ability longer than dry soil (Toole and Toole, 1953 ; Lewis, 1973 ). The soil was wet and the temperature low on Mount Usu (Tsuyuzaki, 1991 ), and thus the activity of bacteria was considered to be low. Therefore, the conditions of wet soil, no light, and low temperature fluctuation of the former topsoil may be adequate for seed survival for many species.

The seed density was similar to the active seed bank observed in the meadow in Tohoku District, Japan (Hayashi and Numata, 1971 ) and abandoned pastures in Hokkaido Island, northern Japan (Tsuyuzaki and Kanda, 1996 ). Those seed banks are persistent (Grime, 1979 ). Species composition in the abandoned pasture resembles the seed bank in the former topsoil of Mount Usu, i.e., there are Poa pratensis, Trifolium repens, Cerastium fontanum, Viola grypoceras, Rumex obtusifolius, Rumex acetosella, and Geum macrophyllum var. sachalinense. Most seeds are small, i.e., 1–2 mm long, in the study of Tohoku District. Nonnative species seem to be common in the various seed banks of seminatural vegetation, such as abandoned meadows and pastures, in Japan. These patterns, i.e., species composition, seed size, density, and spatial patterns of seed bank, appear to have been retained in the seed bank under the volcanic deposits 20 yr after the burial and indicate that conditions are optimal for seed storage and the seed bank will persist longer.

Of species detected in the present study, seeds that have been reported as long lived, i.e., over 20 yr, under (semi-)natural conditions are (Table 3): R. obtusifolius, Trifolium repens, Poa pratensis, Taraxacum officinale, Ranunculus repens, Juncus effusus var. decipiens, and Erigeron annuus. Except for E. annuus and J. effusus var. decipiens, all of these species were also extracted from the former topsoil on Mount Usu 10 yr after the eruptions. Additional species were detected both 10 and 20 yr after the eruptions on Mount Usu; these were Rumex acetosella, Cerastium fontanum, Viola grypoceras, and Geum macrophyllum var. sachalinense (Table 3). The other nine species have not been recorded for seed longevity, or the longevity was reported as <20 yr: Carex oxyandra, Aralia cordata, Hypericum erectum, Hydrocotyle ramiflora, Epilobium cephalostigma, Sagina japonica, Youngia japonica, Eragrostis multicaulis, and Luzula capitata. Of those, the longevity of closely related species are reported as: Hypericum histum and H. perforatum >5 yr (Granstrom 1987; Osumi and Sakurai, 1997 ), and Viola arvensis >20 yr (Chapman and Anderson, 1987 ). The seeds of Sagina decumbens, Luzula parviflora, and L. campestris survive for more than a few decades in various regions (Thompson, Bakker, and Bekker, 1997 ). This suggests that phylogenetic constraints may exist on seed longevity. Seeds and resulting seedlings might be used to determine how the genetic heterogeneity of the seed bank changes under natural storage conditions.


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  		Table 3. Previous reports on species that were found in the "former" topsoil buried underneath volcanic deposits from Mount Usu, northern Japan, 20 yr after the 1977–1978 eruptions

 


   FOOTNOTES
 
1 The authors thank K. Narita and Y. Yamada for field assistance; H. Okada and all staff members of Usu Volcano Observatory for providing facilities; Muroran Forest Management Office for permission to conduct research in a restricted area; and M. A. Leck and E. O. Guerrant Jr. for their critical reading of the manuscript. Funds for this study were partly provided by the Ministry of Education, Science, and Culture of Japan. Back

2 Author for reprint requests (e-mail: tsuyu{at}ees.hokudai.ac.jp ). Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 STUDY AREA AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Baskin C. C. J. M. Baskin 1998 Seeds—ecology, biogeography, and evolution of dormancy and germination. Academic Press, San Diego, California, USA

Bigwood D. W. D. W. Inouye 1988 Spatial pattern analysis of seed banks: an improved method and optimized sampling. Ecology 69: 497-507[CrossRef][ISI]

Chapman D. F. C. B. Anderson 1987 Natural re-seeding and Trifolium repens demography in grazed hill pastures. I. Flowerhead appearance and fate, and seed dynamics. Journal of Applied Ecology 24: 1025-1035[CrossRef][ISI]

Fenner M. 1985 Seed ecology. Chapman and Hall, London, UK

Granström S. 1988 Seed banks at six open and afforested heathland sites in southern Sweden. Journal of Applied Ecology 25: 297-306[CrossRef][ISI]

Grime J. P. 1979 Plant strategies and vegetation processes. Wiley, Chichester, UK

Hara M. 1978 Flora of Mt. Usu. Toya Plant Research Group, Muroran, Japan. (In Japanese.)

Hayashi I. M. Numata 1971 Viable buried-seed population in the Miscanthus-and Zoysia-type grasslands in Japan. Japanese Journal of Ecology 20: 243-252

Kellman M. 1978 Microdistribution of viable weed seed in two tropical soils. Journal of Biogeography 5: 291-300[CrossRef][ISI]

Kivilaan A. R. S. Bandurski 1981 The one hundred-year period for Dr. Beal's seed viability experiment. American Journal of Botany 68: 1290-1292[CrossRef][ISI]

Kramer N. B. F. D. Johnson 1987 Mature forest seed banks of three habitat types in central Idaho. Canadian Journal of Botany 65: 1961-1966

Leck M. A. V. T. Parker R. L. Simpson 1989 Ecology of soil seed banks. Academic Press, San Diego, California, USA

Lewis J. 1973 Longevity of crop and weed seeds: survival after 20 years in soil. Weed Research 13: 179-191[CrossRef][ISI]

Naka K. K. Yoda 1984 Community dynamics of evergreen broadleaf forests in southwestern Japan. II. Species composition and density of seeds buried in the soil of a climax evergreen oak forest. Botanical Magazine, Tokyo 97: 61-79[CrossRef][ISI]

Ohwi J. M. Kitagawa 1983 New flora of Japan. Shibundo, Tokyo, Japan

Osumi K. S. Sakurai 1997 Seedling emergence of Betula maximowicziana following human disturbance and the role of buried viable seeds. Forest Ecology and Management 93: 235-243[CrossRef][ISI]

Poshlod P. S. Jordan 1992 Wiederbeisiedlung eines aufgeforsteten Kalkmagerrasenstandortes nach Rodung. Zeitshrift für Öklogie und Naturschutz 1: 119-139

Roberts T. L. J. L. Vankat 1991 Floristics of a chronosequence corresponding to old field–deciduous forest succession in southwestern Ohio. II. Seed banks. Bulletin of the Torrey Botanical Club 118: 377-384[CrossRef][ISI]

Stöcklin J. M. Fischer 1999 Plants with longer-lived seeds have lower extinction rates in grassland communities 1950–1980. Oecologia 120: 539-543[CrossRef][ISI]

Thompson K. 1986 Small-scale heterogeneity in the seed bank of an acidic grassland. Journal of Ecology 74: 733-738[CrossRef][ISI]

Thompson K. J. Bakker R. Bekker 1997 The soil seed bank of northwest Europe: methodology, density and longevity. Cambridge University Press, Cambridge, UK

Thompson K. J. P. Grime 1979 Seasonal variation on the seed banks of herbaceous species in ten contrasting habitats. Journal of Ecology 67: 893-921[CrossRef]

Toole E. H. E. Brown 1946 Final results of the Duvel buried seed experiment. Journal of Agricultural Research 72: 201-210

Toole V. K. E. H. Toole 1953 Seed dormancy in relation to seed longevity. Proceedings of International Seed Testing Associations 18: 325-328

Tsuyuzaki S. 1987 Origin of plants recovering on the volcano Usu, northern Japan, since the eruptions of 1977 and 1978. Vegetatio 73: 53-58[CrossRef][ISI]

Tsuyuzaki S. 1989 Analysis of revegetation dynamics on the volcano Usu, northern Japan, deforested by 1977–1978 eruptions. American Journal of Botany 76: 1468-1477[CrossRef][ISI]

Tsuyuzaki S. 1991 Survival characteristics of buried seeds 10 years after the eruption of the Usu volcano in northern Japan. Canadian Journal of Botany 69: 2251-2256[CrossRef]

Tsuyuzaki S. 1994 Rapid seed extraction from soils by a flotation method. Weed Research 34: 433-436[CrossRef][ISI]

Tsuyuzaki S. F. Kanda 1996 Revegetation patterns and seedbank structure on abandoned pastures in northern Japan. American Journal of Botany 83: 1422-1428[CrossRef][ISI]

Whittaker R. J. T. Partomihardjo S. Riswan 1995 Surface and buried seed banks from Krakatau, Indonesia: implications for the sterilization hypothesis. Biotropica 27: 346-354[CrossRef][ISI]

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