Vegetation recovery patterns in early volcanic succession
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J. Plant Res. 108 : 241-248, 1995 Journal of Plant Research ~) by The Botanical Society of Japan 1995
Vegetation Recovery Patterns in Early Volcanic Succession
Graduate School of Science and Technology, Niigata University, Niigata, 950-21 Japan
Permanently plots were monitored from 1983 to the present on Mount Usu after the eruptions of 1977-78 which destroyed the pre-eruption vegetation by 1-3 m thick accumulations of ash and pumice in order to clarify the processes and mechanisms of succession. Until now, 163 species were recorded in the summit area. Most of these species were derived from vegetative reproduction throughout the volcanic deposits. Vegeta- tive reproduction plays a major role on increases in cover. Although long-distance seed-dispersal species could immigrate to the crater basin, their cover increase was slow. Seedbank species only established in gullies where the original topsoil was exposed by erosion. Most annuais were supplied by the seedbank in the original topsoil and woody species originated via immigration, suggesting that the source greatly determines the species composition of establishing vegetation. Annual seedlings showed low survival, while overwintering perennial seedlings steadily established. Ground sur- face movements strongly restricted increases in plant cover and the distance from source vegetation was the principal determinant of plant density. Due to differ- ences in disturbance intensity, successional rates were higher in the stable substrates outside gullies and lower on the exposed original topsoil in some gullies.
Key words : Immigration m Mount Usu m Permanent p lot - - Seedbank-- Seedling establishment - - Species composition ~ Vegetative reproduction ~ Volcanic suc- cession
Since the first major ecological theory "ecological succession" was proposed (Clements 1916), a large num- ber of studies have been conducted (see, Glenn-Lewin et al. 1992, Miles and Walton 1993). There are some trends in succession (Whittaker 1975, Tilman 1988, Glenn-Lewin eta/. 1992) : 1) it is a time dependent process with chang- ing vegetation characteristics such as density, cover, and species richness, diversity, and composition, 2) it results from a modification of the stress and disturbance regimes, and 3) it changes ecosystems which are unstable to
* Recipient of the Botanical Society Award of Young Scien- tists, 1994
stable, concerning cover, biomass, and/or diversity infor- mation content.
Plant succession is categorized into primary and secon- dary succession (Clements 1916, Tsuyuzaki 1993a). Pri- mary succession, which occurs following complete destruction of biosystems where the ground surface is covered by rocks and/or inorganic soil substrates (Vitousek and Walker 1989, del Moral and Bliss 1993), is considerably different from secondary succession which may be initiated by burns or abandoned fields (Walker et al. 1982, McCune 1988, Tsuyuzaki et al. 1994). The most important process of primary succession is the accumula- tion of nutrients including nitrogen in the soil (Whittaker 1975, Tilman 1982). Primary succession was previously considered to be principally initiated by blue-green algae, mosses, lichens, etc., while secondary suceession begins with more or less mature soils containing a sizable bank of seeds and vegetative propagules (Crawley 1986, Fenner 1992). Therefore, primary suceession proceeds very slowly in its early stages, due to a sterile ground surface and the lack of a seedbank and vegetative propagules (Tilman 1982, Miles and Walton 1993). Therefore, to clarify successional trends, we must determine plant origins (Tsuyuzaki 1987).
Sites that support primary succession have been pro- vided following glacial retreat (Bormann and Sidle 1990, Matthews 1992), massive landslides (White 1979, Naka- shizuka et al. 1993), and volcanic eruptions (Matson 1990, Tagawa et al. 1985, Whittaker et al. 1986, del Moral and Bliss 1993, Tsuyuzaki and del Moral 1995). To confirm changes over time in successional seres community structure must be assessed for the long-term using per- manent plots, however, these have been rare (Tsuyuzaki 1993). I have annually monitored revegetation on a recently-erupted volcano, Mount Usu, for more than 10 years by measuring vegetation cover and density and also by examining the fates of individual plants belonging to various life form types. The present study was conduct- ed in the crater basin of volcano Usu where many plant species of various life forms were growing. These plants were growing in spite of high seedling mortality induced mainly by ground surface instability.
242 S. Tsuyuzaki
Mount Usu, located on the northernmost Japancse Island, Hokkaido (42~ 140~ is composed of two peaks, O-Usu (727 m) and Ko-Usu (552 m) which are enclosed by a caldera rim and crater basin, with an area of ca. 2 km. The pre-eruption summit area had been covered mostly with forests of Populus maximowiczfi and Betula platyphylla var. japonica and partly with seeded pasture of Dactylis glomerata, Trifolium repens and T. pratense (Tsuyuzaki 1987). In 1977-78 when I was a high school student, the eruptions completely destroyed the vegetation with thick accumulations of tephra. Soon after the eruptions, the northwest slope of O-Usu and inner wall of the caldera rim were covered by a thick layer of volcanic rocks and the crater basin was ovcrlain by volcanic ash and pumice with some deeply eroded gullies in which the original topsoil was exposed. The inner wall of the caldera rim was inhabited by a community of Petasites japonicus var. giganteus and Polygonum sacha- linense, both of which recovered vegetatively soon after the erosion of volcanic deposits, whereas in the crater basin the ash and pumice layer is still thick and revegeta- tion is very slow.
Based on geographical physiognomy, the crater basin was divided into three habitat types. Deep, stable tephra
is the dominant landform outside gullies (i.e., hereafter, T) (Fig. 1). In other locations, erosion was moderated and formed gullies (G) with altered surface conditions but erosion had not reached the original topsoil. Extreme erosion has removed large quantities of ash and pumice, exposing the original surface (E) creating a third type of habitat (Tsuyuzaki 1989a, 1991a). Distance from the cal- dera rim, which was surrogate for the distance from major plant resources, ranged from 50.0 to 400.0 m (Tsuyuzaki and del Moral 1994). Ground surface movements de- creased from -I-41 and --162 cm in 1983 to -I-15 and --2 cm in 1992 in the gullies (positive values mean the accu- mulation of volcanic deposits and negative ones mean the erosion) (Tsuyuzaki 1989a). Ground surface movements were intense in the gullies, but were less than __.10 cm outside the gullies in 1984. On ski slopes in Hokkaido ground surface movements were mostly derived from snow-melt (Tsuyuzaki 1990). Similar processes might occur on Mount Usu (Tsuyuzaki unpublished data).
Organic matter status expressed as loss on ignition ranged from 0.2 to 1.1% in the volcanic deposits and from 2.5 to 13.2% in the original topsoil in 1984 (Tsuyuzaki 1989a), indicating that organic matter content was much greater in E. The loss on ignition of volcanic deposits was less than 5% even in 1994 (Tsuyuzaki unpublished data). These values were only 1/3 of loss on ignition
Species richness and diversity Habitat preference Life form
Contribution and/or Plant origin recovering pace
Medium and high,~-..---
Rich and high
Poor and low ~"
Microhabitat rills cracks
~ egetation ~ Rapid and most reproduction ~ contributive
sion) - ~(R p )
X Seedbank ,,,,,,,,,,,,4~Rapid but decreased \
Ground surface Original topsoil instability
Fig. 1. Revegetation dynamics in the crater basin of the volcano Usu after 1977-78 eruptions. T : outside gully dominated by thick tephra. E: original-topsoil-exposed gully. G: inside gully without original topsoil. Relationships are connected by solid lines (strong relationships are shown by thick solid lines). Woody species were mostly derived from immigration, and annuals were from the seedbank. Annuals, most of which established in the gullies, and well-rooted perennials, that could reach their roots to the original topsoil even on the thick volcanic deposits, utilized nutrients in the original topsoil. Due principally to ground surface movements, most woody species did not establish inside gullies and annuals disappeared after 1989. Ground surface instability restricted plant growth, while perennials could spread their roots by means of long rhizomes and/or stolonierous shoots in spite of the instability. Therefore, perennial species contributed the most to revegetation. Species diversity is higher in habitats T and E than G, due to seedbank and immigrant species.
Vegetation Recovery Patterns in Early Volcanic Succession 243
values from low-productivity abandoned pasture in north- ern Japan (Tsuyuzaki et al. 1994).
Origin of recovering plants
On the summit areas of Mount Usu, 163 vascular plant taxa were observed during the years of 1983 to 1994 (in detail, see Appendix). Four major plant origins were recognized (Tsuyuzaki 1987): vegetative reproduction, seedbank, immigration and artificial introduction as fol- lows (Fig. 1).
Vegetatively-reproducing species Most perennials originated vegetatively from buried
plants throughout the volcanic landscape, e.g., Angelica ursina, Aralia cordata, Petasites japonicus var. giganteus and Polygonum sachalinense. All the species in this group are perennial herbaceous and woody species.
Clonal expansion effectively succeeds in colonization in highly disturbed sites (Fahrig et al. 1994). On Mount St. Helens, vegetative recovery was conspicuous in areas where volcanic deposits were less than 15 cm deep (Antos and Zobel 1985ab). On Mount Usu, P. sachalinense and P. japonicus var. giganteus often recovered from under- ground organs buried by the volcanic deposits more than 50cm deep (Tsuyuzaki 1989a). Therefore, species characteristics such as life form and root system deter- mine the success rates of vegetative recovery. For example, most needle-leaved species could not repro- duce vegetatively after the eruption of Mount St. Helens, while well-rooted perennial herbs Epilobium angustifolium and Anapharis margaritacea rapidly resprouted vigorously from beneath the tephra (Halpern et al. 1990).
Seedbank species Using a K2CO3 floatation technique which can extract
nearly 100% of the viable seeds from soil samples (Tsu- yuzaki 1993b, 1994a), in 1987 viable seeds of 17 species were extracted from the seedbank of original topsoil buried beneath 65-130 cm of volcanic deposits, indicating that seed viability is at least 10 years (Tsuyuzaki 1989b). The most common seedbank species was Rumex obtusifolius. Seed volume of most species tested was less than 2.0 mm 3 and smaller seeds had a greater rate of survival than larger seeds (Tsuyuzaki 1991b). (The vol- ume was calculated by assuming simple ovoid shapes.) Small seeds survive for longer periods in the soil, and their dormancy is frequently associated with a requirement for light (Cook 1980). However, seed survival rates of a few species including R. obtusifolius in the seedbank of Mount Usu were positively correlated with the thickness of volcanic deposits, suggesting that stable soil tempera- ture with little diurnal fluctuations allowed for long-term survival (Thill et al. 1985, Tsuyuzaki 1991b). In addition, the species composition of the seedbank might be related to the pre-eruption vegetation, although the relation was weak (Tsuyuzaki 1989b). Based on these analyses, I concluded that at least 14 species were derived from the
seedbank (Tsuyuzaki 1994b). While the distribution of seedbank species was
restricted to the deeply eroded gullies of the crater basin where the original topsoil became exposed, these species greatly contributed to increased species richness there (Tsuyuzaki 1989c). The seedbank included both annual and perennial herbaceous species. All the annuals except for Senecio vulgaris were derived from the seed- bank, indicating that the seedbank is an important deter- minant of initial stages of revegetation (Tsuyuzaki 1989c, 1994b). Buried seeds contribute greatly to secondary succession starting with abandoned pastures, post-fire forests, etc. (Archibold 1981, Hill and Stevens 1981). Due to the seedbank containing a large number of the seeds of annuals, secondary succession often starts with the dominance of annual plants (Leck et al. 1989). Revegetation processes on Mount Usu suggest that typi- cal secondary succession could be recognized if seed- rich soil re-appears immediately after the disturbance.
Immigration Most immigrating species produce long-distance wind-
dispersed seeds. Most. woody species such as Salix hultenii var. angustifolium, Populus maximowiczii, Betula plaryphylla var. japonica, and Larix kaempferi were immi- grants into the crater basin. Herbaceous species, e.g., Senecio vulgaris, Anaphalis margaritacea var. angus- tifolior, Aster ageratoides var. ovatus, and Epilobium montanum also recovered via immigrant seeds (Tsuyuzaki 1987). Animal-dispersed species such as Prunus sar- gentii and Fragaria vesca were infrequently observed and they did not persist in the crater basin.
Floristic sources surrounding the crater basin strongly determined the rate of vegetation recovery (Tsuyuzaki 1991a, 1994b). For example, due to the paucity of annuals in the intact vegetation, annuals were rare in the crater basin. Similar trends were also observed after the erup- tion of Mount St. Helens (del Moral 1988). Vegetation recovery was faster in areas where plant sources were closely available (Wood and del Moral 1987, del Moral and Wood 1988). Therefore, wind-dispersal is often the most important determinant of vegetation recovery (Dale 1985, Nakashizuka et al. 1993). On newly-emerged islands such as Anak Krakatau in Indonesia and Surtsey in Iceland, all seeds must immigrate from outside of the island. In these cases, water-dispersal as well as wind -dispersal contribute to make up the new species compo- sition (Fridriksson 1992).
Artificially-introduced species A few grass and legumes were introduced for artificial
erosion control. The major species were Festuca rubra and F. elatior (Tsuyuzaki 1987). These species were aerial sprayed shortly after the eruptions, and to a much lesser extent invaded from outside of the caldera rim. However, their total cover was very small, i.e., less than 3% even in 1989 (Tsuyuzaki 1989a), indicating that the effects of artificial introduction to prevent ground surface
244 S. Tsuyuzaki
movements are minimal.
Determinants of vegetation dynamics
Based on eight environmental factors, loss on ignition of volcanic deposits collected from the ground surface, tephra deposition and erosion, distance from the caldera rim, relative elevation difference, and three nominal hab- itat variables (T, G and E), canonical correspondence analysis (CCA) was conducted (Tsuyuzaki and del Moral 1994). This analysis evaluates the influence of environ- mental variables on vegetation development patterns (ter Braak 1986, Palmer 1993). Plant density and plant cover were analyzed separately because these two parameters fluctuated somewhat differently over time. As expected, the CCA suggested that the environmental factors which influence plant density and cover differ. Distance from the source of colonizing species source, i.e., from the caldera rim, primarily affected plant density, while erosion strongly affected cover. Therefore, plant growth which is represented by fluctuation in cover seems to be principally limited by ground surface stability. In addition, the pre- eruption surface played a special role in vegetation devel- opment because the original topsoil supplied both nutri- ents and seedbank species. In an Alaskan floodplain, many woody species could establish even in the early stages of primary succession, due to the species compo- sition of the surrounding vegetation (Walker et al. 1986). Therefore, species composition in the early stages of succession seems to be somewhat determined by that of the source vegetation (Tsuyuzaki 1989a, 1993a).
Diverse microhabitat characteristics, e.g., large parti- cles on the ground surface, microtopography such as rill development, and dead lupine patches, promote seedling establishment (del Moral and Bliss 1993). Since seeds are often entrapped by cracks and rills, seedlings fre- quently emerged in such sites even under low nutrient conditions (Smathers and Muller-Dombois 1974, Cham- bers 1991). On Mount Usu, many seedlings emerged in areas where the large volcanic deposits were accumulat- ed and inside rills (Tsuyuzaki unpublished data). There- fore, the availability of safe sites for germination and establishment may limit the rate of primary succession (Wood and Morris 1990).
Total cover increased annually in the crater basin, however, the rates of increase differed among the three habitats, T, G and E (Tsuyuzaki 1991a) (Fig. l). The species with the greatest cover were perennials, due to the rapid expansion of long rhizomes and/or stoloniferous shoots. In habitat G their cover increased dramatically probably because the layer of volcanic deposits was thinner than at T and the intensity of ground surface movements was more moderate than at E. Most annual species disappeared after 1989 due perhaps to low fruiting success and/or fragile root systems, whereas perennial
species derived from the seedbank yearly increased in cover (Tsuyuzaki 1994b). Of these, nitrogen-fixing stoloniferous perennials, Trifolium repens and Lotus cor- niculatus var. japonica, both of which were derived from the seedbank only, gradually increased in cover (Tsuyuza- ki 1994b). Nitrogen-fixing species such as legumes and alders are often dominant in the early stages of primary succession (Vitousek et al. 1987, Walker 1993). Woody plants such as willows, birches and alders also immigrat- ed from the external environment, but they grew slower than the perennial herbs. In contrast to gradual increase in cover, the large fluctuations in density suggests that mortality is high in young seedlings but relatively low once plants establish (Tsuyuzaki 1989a). The survival rates of annual seedlings were 20-40% in a permanent plot out- side the gully from 1983 to 1987, while seedlings once they overwintered persisted there. There were no clear differ- ences in survival rates between herbaceous and woody plants.
Although rate of vegetation change is one of the impor- tant characteristics of both primary and secondary suc- cession, analyses of successional rates are rare. This may be because of difficulties in generalizing changes to different vegetation properties (Bornkamm 1981, Prach 1993). Evaluations of stability, diversity and evenness have been applied to various communities (e.g., Peet 1974, McCune 1988, del Moral and Wood 1988). Fluctua- tions in these properties are considered to express trends in successional state over time. Percentage similarity PS) and community cocfficient (CC) were originally used to express inter-community heterogeneity (Dahl and Hadac 1941, Sorensen 1948), and can be used to express rates of vegetation change during succession (Bornkamm 1981). If a chronofunction v=f(t) is used for the descrip- tion of vegetation, a stable situation at the end of a succession is indicated by dv/dt=O. It was proposed that the terminal stage of suceession is reached when dv/ dt is less than 5% (Tagawa 1964, Bornkamm 1981). Although species diversity often increases with time in the early stages of succession (Drury and Nisbet 1973, del Moral and Bliss 1993), species diversity remained low and did not change over time on Mount Usu due principally to low species richness and evenness (Tsuyuzaki 1991a). Therefore, species richness, diversity and evenness do not yet show a clear trend. Instead of using those diversity indicators, successional changes, expressed as PS and CC, showed the fastest change in habitat T and the slowest in habitat G (Tsuyuzaki 1991a). Furthermore, the year-to-year changes were more than 20% in all of the habitats, suggesting that the vegetation status was still unstable in spite of showing stable, low diversities (Tsuyuzaki 1991a).
A volcano is a unique site for monitoring plant succes- sion because there are wide ranges in stresses and disturbances (Tsuyuzaki 1991a, del Moral and Bliss 1993).
Vegetation Recovery Patterns in Early Volcanic Succession 245
Secondary succession on ski slopes shows similar trends to volcanic succession ; viz. large ground surface move- ments occur on the slope, bare ground remains unvegetat- ed for a long time, and distance from plant sources is related to revegetation patterns (Tsuyuzaki 1990, 1993c, 1994c, 1995). Therefore, trends in the early stages of primary and secondary succession might be similar under certain conditions such as steep slopes.
Thus far, there has been little information on a flora prior to the eruption on any volcano, even at Mount St. Helens where numerous plant ecologists surveyed. The per- iodicity of eruption on Mount Usu ranges from 30 to 40 years, inferring that the next eruption will occur in a few decades. The flora list is necessary to estimate the effects of eruptive disturbances on post-eruption vegeta- tion. I list here the taxa observed in the crater basin, inner-wall of the caldera rim and northwest face of O-Usu (Appendix).
I wish to express sincere thanks to S. Yoshida, K. Ito, M. Kurogi, S. Higashi, M. Haruki, T. Sato, M. Maeshima, and S. Hino for their useful advice, and all staff members of Usu Volcano Observatory and many colleagues for their field assistance. Cordial thanks are also due to J.H. Titus for his critical readings of the manuscript. This work is partly supported by Grants from the Ministry of Education, Science and Culture of Japan.
Antos, A.J. and Zobel, D.B. 1985a. Recovery of forest understories buried by tephra from Mount St. Helens. Vegetatio 64 : 103-111.
Antos, A.J. and Zobel, D,B. 1985b. Plant form, develop- mental plasticity and survival following burial by volcanic tephra. Can. J. Bot. 63 : 2083-2090.
Archibold, O.W. 1981. Buried viable propagules in native and adjacent agricultural sites in central Saskatch- ewan. Can. J. Bot. 59: 701-706.
Bormann, B.T. and Sidle, R.C. 1990. Changes in produc- tivity and distribution of nutrients in a chronosequ- ence at Glacier BayNational Park, Alaska. J. Ecol. 78 : 561-578.
Bornkamm, R. 1981. Rates of change in vegetation dur- ing secondary succession. Vegetatio 47 : 213-220.
Chambers, J.C. 1991. Seed entrapment in alpine eco- system: effects of soil particle size and diaspore morphology. Ecology 72 : 1668-1677.
Clementa, F.E. 1916. Plant Succession. Carnegie inst., Washington.
Cook, R. 1980. The biology of seeds in the soil. In O.T. Solbrig, ed. Demography and Evolution in Plant Population. Blackwell Scientific Publishers, Oxford. pp. 107-129.
DaM, E. and Hadac, E. 1941. Strandgessellschaften der Insel Ostoy im Oslofiord. Nytt. Mag. Naturv. 82: 251-312.
Dale, V.H. 1989. Wind dispersed seeds and plant recov- ery on the Mount St. Helens debris avalanche. Can.
J. Bot. 67: 1434-1441. del Moral, R. 1988. The high elevation flora of Mount St.
Helens, Washington. Manrono 35 : 309-319. del Moral, R. and Bliss, L.C. 1993. Mechanisms of pri-
mary succession : insights resulting from the eruption of Mount St. Helens. Adv. Ecol. Res. 24 : 1-66.
del Moral, R. and Wood, D.M. 1988. Dynamics of herba- ceous vegetation recovery on Mount St. Helens, Washington, USA, after a volcanic eruption. Vegetatio 74 : 11-27.
Drury, W.H. and Nisbet, I.C.T. 1973. Succession. J. Arnold Arbor., Harvard Univ. 54: 331-368.
Fahrig, L., Coffin, D.P., Lauenroth, W.K and Shugart, H.H. 1994. The advantage of long-distance clonal spreading in highly disturbed habitats. Evolutionary Ecol. 8 : 172-187.
Fenner, M. 1992. Seeds: the Ecology of Regeneration in Plant Communities. C.A.B. International, Walling- ford.
Fridriksson, S. 1992. Development of the ecosystem on Surtsey with references to Anak Krakatau. Geo Journal 28 : 287-291.
Glenn-Lewin, D.C., Peer, R.K and Veblen, T.T. 1992. Plant Succession:Theory and Prediction. Chap- man & Hall, London.
Griggs, F.R. and Ready, D. 1934. Growth of liverworts from Katmai in nitrogen-free media. Amer. J. Bot. 21 : 285-277.
Halpern, C.B., Frenzen, P.M., Mean, J.E. and Franklin, J.F. 1990. Plant succession in areas of scorched and blown-down forest after the 1980 eruption of Mount St. Helens, Washington. J. Veg. Sci. 1: 181-194.
Hill, M.O. and Stevens, P.A. 1981. The density of viable seed in soils of forest plantations in upland Britain. J. Ecol. 69: 693-709.
Leck, M.A., Parker, V.T. and Simpson, R.L. 1989. Ecol- ogy of Soil Seed Banks. Academic Press., Inc., San Diego.
Matson, P. 1990. Plant-soil interactions in primary suc- cession at Hawaii Volcanoes National Park. Oecologia 85 : 241-246.
Marthews, J.A. 1992. The Ecology of Recently-Deg- laciated Terrain : a Geoccological Approach to Gla- cier Forelands and Primary Succession. Cambridge University Press, Cambridge.
McCune, B. 1988. Ecological diversity in north American pines. Amer. J. Bot. 75 : 353-368.
Miles, J and Walton, D.W.H. 1993. Primary Succession on Land. Blackwell Scientific Publishers, London.
Nakashizuka, T., lida, S., Suzuki, W. and Tanimoto, T. 1993. Seed dispersal and vegetation development on a debris avalanche on the Ontake volcano, central Japan. J. Veg. Sci. 4: 537-542.
Ohwi, J. 1975. Flora of Japan (rev. edn). Shibundo, Tokyo.
Palmer, M,W. 1993. Putting testing in even better order : the advantages of canonical correspondence analy- sis. Ecology 74 : 2215-2230.
Peet, R.K 1974. The measurement of species diversity. Ann. Rev. Ecol. Syst. 5: 285-307.
Prach, K, 1993. On the rate of suceession. Oikos 66:
246 S. Tsuyuzaki
343-346. Smathers, G.A. and Muller-Dombois, D. 1974. Invasion
and Recovery of Vegetation after a Volcanic Eruption in Hawaii. National Park Service Science Mono- graph Number 5.
S~rensen, T. 1948. A method of establishing groups of equal amplitude in plant sociology based on similarity of species content. Det Kong. Danske Vidensk. Selsk. Biol. Skr. (Copenhagen) 5 : 1-34.
Tagawa, H. 1964. A study of volcanic vegetation in Sakurajima, southwest Japan I. Dynamics of vege- tation. Mem. Fac. Sci. Kyushu Univ., Ser. E. (Biol.). 3 : 165-228.
Tagawa, H., Suzuki, E., Pattomihardjo, T. and Suriadarma, A. 1985. Vegetation and succession on the Kra- katau Islands, Indonesia. Vegetatio 60: 131-145.
ter Braak, C.J.F. 1986. Canonical correspondence ana- lysis: a new eigenvector technique for multivariate direct gradient analysis. Ecology 67 : 69-77.
Thill, D.C. Zamora, D.L. and Kambitsch, D.L. 1985. Ger- mination and viability of common cuprina (Cuprina vulgaris) achenes buried in the field. Weed Sci. 33 : 344-348.
Tilman, D. 1982. Resource Competition and Community Structure. Princeton University Press, Princeton.
Tsuyuzaki, S. 1987. Origin of plants recovering on the volcano Usu, northern Japan, since the eruptions of 1977 and 1978. Vegetatio 73 : 53-58.
Tsuyuzaki, S. 1989a. Analysis of revegetation dynamics on the volcano Usu, northern Japan, deforested by 1977-78 eruptions. Amer. J. Bot. 76 : 1468-1477.
Tsuyuzaki, S. 1989b. Buried seed populations on the volcano Mr. Usu, northern Japan, ten years after the 1977-78 eruptions. Ecol. Res. 4: 167-173.
Tsuyuzaki, S. 1989c. Contribution of buried seeds to revegetation after eruptions of the volcano Usu, northern Japan. Bot. Mag. Tokyo 102 : 511-520.
Tsuyuzaki, S. 1990. Species composition and soil ero- sion on a ski area in Hokkaido, northern Japan. Environ. Manag. 14: 203-207.
Tsuyuzaki, S. 1991a. Species turnover and diversity dur- ing early stages of vegetation recovery on the vol- cano Usu, northern Japan. J. Veg. Sci. 2: 301-306.
Tsuyuzaki, S. 1991b. Survival characteristics of buried seeds 10 years after the eruption of the Usu Volcano in northern Japan. Can. J. Bot. 69 : 2251-2256.
Tsuyuzaki, S. 1993a. Is volcanic succession primary succession ? Biological Sciences, Tokyo 45: 177- 181. (in Japanese).
Tsuyuzaki, S. 1993b. Seed viability after immersion in K2003 solution. Seed Sci. Teohnol. 21 : 479-481.
Tsuyuzaki, S. 1993c. Recent vegetation and prediction of the successional sere on ski grounds in the high- lands of Hokkaido, northern Japan. Biol. Conserv. 63 : 255-260.
Tsuyuzaki, S. 1994a. Rapid seed extraction from soils by a flotation method. Weed Res. 34 : 433-436.
Tsuyuzaki, S. 1994b. Fate of plants from buried seeds on volcano Usu, Japan, after the 1977-78 eruptions. Amer. J. Bot. 81 : 395-399.
Tsuyuzaki, S. 1994c. Environmental deterioration result-
ing from ski resort construction in Japan. Environ. Conserv. 21 : 121-125.
Tsuyuzaki, S. 1995. Ski slope vegetation in central Honshu, Japan. Enviorn. Manage. (in press).
Tsuyuzaki, S. and del Moral, R. 1994. Canonical cor- respondence analysis of early volcanic succession on Mt Usu, Japan. Ecol. Res. 9 : 143-150.
Tsuyuzaki, S. and del Moral, R. 1995. Species attributes in early primary succession on volcanoes. J. Veg. Soi. (in press).
Tsuyuzaki, S., Kanda, F. and Narita, K. 1994. Revegeta- tion patterns on an abandoned pasture in northern Japan. Acta Oecologica 15 : 461-467.
Vitousek, P.M. and Walker, L.R. 1989. Biological inva- sion by Mirica faya in Hawaii plant demography, nitrogen fixation, ecosystem effects. Ecol. Monogr. 59 : 247-265.
Vitousek, P.M., Walker, L.R., Whiteaker, D., Muller-Dom- bois, D. and Matson, P.A. 1987. Biological invasion by Mirica faya alters ecosystem development in Hawaii. Science 238 : 802-804.
Walker, L.R., Zasada, J.C. and Chapin III, F.S. 1986, The role of life history processes in primary succession on an Alaskan floodplain. Ecology 67 : 1243-1253.
Walker, L.R. 1993. Nitrogen fixers and species replace- ments in primary succession. In J. Miles and D.W.H. Walton, eds. Primary Succession on Land. Black- well Scientific Publishers, London. pp. 249-272.
Whittaker, R.H. 1975. Communities and Ecosystems (2nd edn.). Macmillan, New York.
Whittaker, R.J., Bush, M.B. and Richards, K. 1989. Plant recolonization and vegetation succession on the Karkatau Islands, Indonesia. Ecol. Monogr. 59 : 59- 123.
Wood, D.M. and del Moral, R. 1987. Mechanisms of early primary succession in subalpine habitats on Mount St. Helens. Ecology 68: 780-790.
Wood, D.M. and Morris, W.F. 1990. Ecological con- straints to seedling establishment on the Pumice Plains, Mount St. Helens, Washington. Amer. J. Bot. 77 : 1411-1418.
(Received January 9, 1995 : Accepted April 11, 1995)
Vascular plants collected in the volcano Usu during the years of 1983 and 1994. O, B, and C indicate the location of north-west slope of O-Usu, crater basin, and inner-wall of caldera rim, respectively. Nomenclature follows Ohwi (1975).
Division Pteridophyta Family Equisetaceae
Equisetum arvense i-0, B, C] Family Aspidiaceae
Dryopteris austriaca E O, C ] Dryopteris crassirhizoma E 0, B] Matteuccia struthiopteris [0, B ]
Vegetation Recovery Patterns in Early Volcanic Succession 247
Subdivision Gymnospermae Family Pinaceae
Larix kaempferi EO, B] Subdivision Angiospermae Class Monocotyledoneae Family Gramineae
Agrostis alba EO, B] Agrostis scabra I-O] Alopecurus aequalis var. amurensis i-B] Calamagrestis epigeios I-O, C] Calamagrostis pseudo-phragmites FO] Dactylis glomerata i-O] Dig#aria adscendens I-B, C] Festuca elatior I-O, B, C] Festuca ovina I-O, B, C] Festuca rubra vat. rubra EO, B, C] Lolium perenne I-B, C] Miscanthus sinensis I-O, B, C] Phleum pratense [O] Poa annua i-B]
Family Cyperaceae Carex leucochlora EO, B, C] Carex flavocuspis [O] Carex lanceolata [O] Carex Iongerostrata i-O] Carex ryngbyei  Carex oxyandra I-O, B, C]
Family Juncaceae Juncus effusus var. decipiens I-B] Juncus fauriensis EB] Luzula capitata EO, B]
Family Liliaceae Polygonatum odoratum var. pluriflorum I-C] Trillium tschonoskii EC-I
Family Orchidaceae Spiranthes sinensis I-B] Gymnadenia camtschatica EB, C]
Class Dicotyledoneae Subelass Choripetalae Family Salicaceae
Populus davidiana I-BI Populus maximowiczii iO, B, C] Salix hultenfi var. angustifolia [0, B, C~ Salix integra Thunb. I-O, B, C] Salix miyabeana EB] Salix reinii [O] Salix sachalinensis I-O, B, C]
Family Betulaceae Alnus hirsuta I-O, B, C] Alnus maximowiczfi i-O, B, C] Betula ermanii [0, B] Betula maximowicziana EO, B] Betula platyphylla var. japonica I-B]
Family Ulmaceae Ulmus davidiana var. japonica I-C] Ulmus davidiana var. japonica f. suberosa I-C] Ulmus laciniata I-C]
Morus bombycis E C ] Family Urticaceae
Boehmeria spicata EO, C] Family Polygonaceae
Polygonum aviculare EB] Polyognum cuspidatum EO, B] Polygonum Iongisetum EO, B] Polygonum sachalinense iO, B, C] Polygonum thunbergfi ro] Rumex acetosella [B] Rumex obtusifolius IB-I
Family Chenopodiaceae Chenopodium centrorubrum [B]
Family Caryophyllaceae Cerastium holosteoides var. angustifolium rB] Moehringia lateriflora ro, B] Stellaria fenzlii i-B]
Family Ranunculaceae Ranunculus repens [B] Ranunculus quelpaertensis var. glaber [B]
Family Magnoliaceae Magnolia obovata [C-I
Family Cruciferae Arabis lyrata var. kamtschatica I-O, B] Arabis pendula FB] Arabis serrata vat. glauca EB, C] Cardamine flexuosa EO, B, C-J Cardamine flexuosa var. fallax I-B, C] Rorippa islandica [B] Turritis glabra I-C]
Family Saxifiagaceae Astilbe thunbergii var. congesta I-O, B] Hydrangea paniculata i-O, B, C] Hydrangea petiolaris I-O, C] Schizophragma hydrangeoides C]
Family Rosaceae Aruncus dioicus vat. tenuifolius I-O, C] Geum aleppicum I-B, C] Geum japonicum I-BI Geum macrophyllum var. sachalinense I-O, B] Fragaria iinumae i-O, C~] Fragaria vesca I-B] Potentilla freyniana rB] Prunus sargentii I-B, C] Rosa multiflora I-C] Rubus phoenicolasius I-C] Sorbus alnifolia rc] Sorbus commixta I-C]
Family Leguminosae Desmodium oxyphyllum i-C] Lespedeza bicolor [ C ] Lotus comiculatus vat. japonicus iB] Medicago lupulina EB] Robinia pseudo-acacia I-B, C] Trifolium hybridum I-B, C] Trifolium pratense IB] Trifolium repens I-O, B]
248 S. Tsuyuzaki
Phellodendron amurense var. sachalinense i-C] Family Anacardiaceae
Rhus ambigua I-O, C] Rhus trichocarpa i-C]
Family Celastraceae Celastrus orbiculatus E O, c ] Euonymus sieboldianus I-B, C]
Family Aceraceae Acer japonicum FB, C] Acer mono I-B, C] Acer mono var. mayrii I-C]
Family Vitaceae Vitis coignetiae i-C]
Family Tiliaceae Tilia japonica I-C]
Family Actinidiaceae Actinidia arguta I-C]
Family Guttiferae Hypericum erectum I-B]
Family Violaceae Viola grypoceras I-O, B] Viola phalacrocarpa FB] Viola rossii l-B]
Family Elaeagnaceae Elaeagnus umbellata FB, CI
Family Onagraceae Epilobium angustifolium I-B, C] Epilobium cephalostigma EBI Epilobium dielsfi FB] Epilobium montanum ro, B, C] Epilobium palustre var. lavandulaefolium FB, C] Oenothera biennis [O, B, C-I
Family Araliaceae Aralia cordata I-O, B, C] Aralia elata I-C] Kalopanax pictus [ C ]
Family Umbelliferae Angelica ursina FC] Angelica edulis ro, c] Pleurospermum camtschaticum [C] Torilis japonica F C ]
Subclass Gamopetalae Family Oleaceae
Fraxinus lanuginosa EC-I Family Boraginaceae
Myosotis palustris FB] Myosotis svlvatica EBI
Family Labiatae Stachys japonica var. intermedia I-O~
Family Scrophulariaceae Veronica arvensis i-B] Veronica schmidtiana [0, B]
Family Plantaginaceae Plantago asiatica iB, C] Plantago camtschatica I-O]
Family Caprifoliaceae Lonicera morrowii EO, B, C] Sambucus sieboldiana var. miquelii l-O] Viburnum dilatatum FC] Viburnum sargentii EC]
Family Valerianaceae Patrinia villosa FCI
Family Compositae Adenocaulon himalacium i-B-I Ambrosia artemisiaefolia var. elatior I-B] Anaphalis margaritacea var. angustior EO, B, C] Artemisia japonica I-C] Artemisa montana FO, B, C] Aster ageratoides var. ovatus f. yezoensis I-B, CI Aster glehnfi I-B, C] Aster scaber l-B, Cl Cacalia hastata var. orientalis I-B, C] Erigeron annuus FB, CI Erigeron canadensis I-B] Eupatorium chinense vat. sachafinense EO, B, C] Eupatorium chinense var. simplicifolium ro, c] Hieracium umbellatum l-B] Hypochaeris radicata I-B3 Ixeris dentata l-B ~ Leibnitzia anandria I-B] Petasites japonicus var. giganteus EO, B, C] Picris japonica E O, B, C ] Senecio cannabifolius I-B, C] Senecio vulgaris I-B] Solidago virgaurea var. leiocarpa i-C] Sonchus asper l-B] Taraxacum hondoense I-C] Taraxacum officinale I-B, C] Youngia denticulata i-B] Youngia japonica FB]