A JOURNAL ON TAXONOMIC BOTANY PLANT SOCIOLOGY AND ECOLOGY REINWARDTIA Editors SOEDARSONO RISWAN MIEN A RIFAI ELIZABETH A. WIDJAJA Published by HERBARIUM BOGORIENSE BALAI PENELITIAN DAN PENGEMBANGAN BOTANI PUSAT PENELITIAN DAN PENGEMBANGAN BIOLOGI — LIPI BOGOR, INDONESIA Reinwardtia Vol. 11, Part 1, 1 - 55 5 February 1992 IO ISSN 0034 - 365 X REINWARDTIA Vol. 11, Part 1, pp. 1 - 11 (1992) SEED BANKS IN A SUBTROPICAL RAIN FOREST ROCHADI ABDULHADI "Herbarium Bogoriense", Puslitbang Biologi, Bogor ABSTRACT The seasonal populations and vertical distribution of seed banks in a subtropical rain forest were assessed,. No seasonal variations were indicated in either the species composition or the size of seed bank over a year period. The numbers of seeds were 550 — 603 m -2 , and mostly composed of secondary species. This population decreased with increasing soil depths. ABSTRAK Populasi bank biji di tanah hutan subtropika basah ditelaah, meliputi variasi musim dan persebarannya secara vertikal Populasi bank biji tidak memperlihatkan adanya variasi musiman selama satu tahun baik komposisi maupun jumlah bijinya. Jumlah biji tercatat sebanyak 550 — 603 m-2, dan sebagian besar merupakan jenis-jenis sekunder, Populasi bank biji ini menurun sejalan dengan kedalaman tanah yang semakin bertambah. INTRODUCTION The seed bank is defined as the number of viable seed stored in or on the soil. The occurence of seed bank beneath the rain forest communities was likely firstly demonstrated by Symington (1933), although he ignored whether those seeds were long term members of a dormant pool or had only recently arrived. More recently many other scientists such as Keay (1960), Guevara and Gomez-Pompa (1972), Liew (1973), Checke et al. (1979), Hall and Swaine (1980), Hopkins and Graham (1983), Knight (1985) and Graham (1988) have attempted to elucidate the size and composition of seed banks in rain forests in the tropics. The conclusion emerging from this work has been that the viable seed bank is dominated by pioneers or secondary species. However, no similar studies have been carried out in sub-tropical rain forests. The present study was designed to assess the seasonal size, composition and the vertical distribution of the viable seed bank in an undisturbed sub- tropical rain forest. REINWARDTIA [VOL. 11 STUDY AREA AND METHODS Study was carried out in the vicinity of O'Reilly's Guest House, the Lamington National Park (28° 14' S and 153° 7' E), Queensland (Figure 1). The topography is dominated by a series plateaux and intervening valleys (Lamb, 1980) and lies at 900 m above sea level. The soil is a kraznozem derived form tertiary basalt (Stevens, 1977). Rainfall in the area is annually about 1,880 mm. It is seasonal and dry conditions are likely to exist during the winter (July-October). The wettest months are recorded for the summer between November and April. Vegetation in the study area is subtropical rain forest, which is classi- fied as Complex Notophyll Vine Forest (Webb, 1968). It is close to the young regrowth forest and pasture area. Soil samples were collected over a 12 month period, at three times (August 1985, January 1986 and July 1986). On each occasion, ten soil samples of 50 x 25 x 5 cm were collected from 5 transects. Successive soil samples of 50 x 25 cm in area with a depth of 5 cm were also collected to a total depth of 25 cm in February 1986. Five replications were collected, one sample from each' transect. To avoid any possibility of contamination from adjacent soil, the point sample was trenched before- hand. Soil samples were taken to the glass house immediately. On the following day of each sampling time, every soil sample was mixed and all live vegetative material was carefully removed. Each sample was then spread over vermiculite in two germination trays (each being 34 x 28 cm) in the glass house. Six control trays containing steam sterilized soil were placed among the samples to monitor contamination. The soil samples were kept moist by daily watering in the early morning and late afternoon. Additionally, to help promote the germination of buried seed, the soil was subsequently carefully disturbed twice i.e., on week 15 and week 30. Seedling emergence was monitored weekly for 40 weeks. Each seedling emerging was marked by a coloured toothpick coded to show the date. Samples of all seedling types were transplanted to pots of 15 cm diameter, and allowed to mature until they could be identified. Herbarium specimens were made of representative samples of each species. RESULTS During the observation period in the glass house two species Cardamine hirsuta and Portulaca oleracea were found in the control trays. Both species are common weeds and grow nearby outside the glass house. These seedlings, therefore, have been removed from the records discussed below. 1992] ROCHADI ABDULHADI : Seed Banks in a Subtropical Forest Size and composition of seed bank The size of the viable seed bank is expressed on a per m2 basis and is the mean of the germination recorded for the 10 soil samples at each site over 40 weeks. The variation of the seed bank over a year is given in Table 1. The number of seeds slightly decreased from 603 per m2 in August 1985 to 545 per m2 in July 1986. However, results of an analysis of variance of the data obtained from the three sampling times indicated no significance differences between the sampling times (P>0.1). A similar result was also found for each life form. Table 1. Seasonal variation in number of seed in seed bank according to their life forms (means of 10 replicates). Primary trees Secondary trees Vines Herbs Shrubs Other Number of August '8 5 56.8 175.2 191.2 131.2 3 7 . 6 12.2 seeds per m2 January '86 53.6 210.4 288:6 89.6 264. 17.6 July '86 64.8 208.8 135.2 96.0 31.2 14.4 Significance level NS NS NS NS NS NS Total 603.2 583.2 550.4 NS NS. Not significantly different (P>0.05) The species richness of soil seed banks in undisturbed forest was similar in the dry season and the wet season (Table 2). The numbers of species present in August 1985, Januari 1986 and July 1986 were 58, 56 and 52 species respectively. Additionally, a similar number of species was also recorded for each life form. The floristic similarity in the wet season (Feb- ruary 86) and two dry seasons using Sorensen Index was 74 — 78%. The floristic similarity in the two dry seasons was 70%. REINWARDTIA [VOL. 11 SOUTH PACIFIC Surfers Paradice OCEAN Burteigh Heads 30km Figure 1. Map showing the location of the Lamington National Park and O'Reilly's Guest House in South-east Queensland. 1992] R O C H A D I ABDULHADI : Seed Banks in a Subtropical Forest Table 2. Seasonal variation of number of species according to their life forms (totals of 10 replicates). Primary trees Secondary trees Vines Herbs Shrubs Other Total August 5 12 13 19 6 3 58 Number of species per 1 1985 January 1986 5 9 12 20 7 3 56 .25 m2 July 1986 5 12 11 16 6 2 52 Table 3. The numbers of seeds germinating (per m2) from various soil depths and the correlation between these numbers (means of 5 replicates) and soil depths. Depth (cm) Primary trees Secondary trees Shrubs Vines Herbs Grass Unknown Total * =P<0.05 ** = P<0.01 Number 0 - 5 54.4 152.0 38.4 193,6 97.6 3.2 6.4 555.2 of seed 5—10 0 27.2 12.8 32.0 38.4 0 0 99.2 per square 10—15 0 12.8 16.0 11.2 17.6 0 0 57.6 metre 15—20 0 4.8 8.0 9.6 6.4 0 0 28.8 20—25 0 3.2 3.2 1,6 1.6 0 0 9.6 Correlation coefficient — - 0.7990* — 0.8746** - 0.7906* — 0.9047** — — — 0.8021* Vertical distribution of seed banks The numbers of seed and the numbers of species both drastically dec- reased with increasing soil depth. However, number of species, especially herbs, were proportionally found at depths of more than 10 cm (Figure 2). Of 50 species recorded in the all level of depths, one secondary tree species, two vines, three shrubs and three herbs were distributed to at least 20 cm deep (Figure 3). These were Dendrocnide excelsa, (the only tree), Cle- R E I N W A R D T I A [ V O L . 1 1 Table 4. A comparison of soil seed banks in rain forest communities. Authors Keay(1960) Guevara & Go- mex Pompa (1972) Cheke et al. (1979) Hall & Swaine (1980) Uhl & Clark (1983) Hopkins & Gra- ham (1983) Putz & Apannah (1987) Present study Location Nigeria Mexico Thailand Ghana Venezuela North Queensland Malaysia South-east Queensland Vegetation type LRF LRF, site 1 LRF, site 2 LRF SDF E F LRF (mixed forest) L R F (caatinga) CMVF, site 1 NMVF, site 2 MMVF, site 3 CMVF, site 4 LRF CMVF Sample area (cm"2) 5200 640 (x8 repeats) 640 (x 8 repeats) 10000 10000 10000 5200 12000 15000 15000 15000 15000 4241 12500 (x3 repeats) Number of species 4 2 13 26 27 30 & 43 17 & 22 13 14 64 64 79 60 30 52 — 58 Number of seeds (m-2) 233 175 — 689 344 — 862 182 633 & 696 45 & 163 180 200 588 516 1069 593 131 . 550 — 603 LRF. Lowland rain forest SDF. Semideciduous forest EF. Evergreen forest CMVF. Complex Mesophyll Vine forest NMVF. Nothophyll-Mesophyll Vine forest MMVF. Mixed Mesophyll Vine forest matis glycinoides, Rubus rosifolius, Conyza sp., Hydrocotyle pedicellosa, Urtica incisa, Solarium aviculare, and Solanum inaquilaterum. Three of these species occurred at 25 cm deep. All these species had seeds smaller than two mm in size. No primary species occurred below five cm deep. The number of seeds germinating, are given in Table 3. For several life form groups these numbers were negatively correlated with soil depth. REINWARDTIA [VOL. 11 5 10 15 20 25 0 5 10 15 20 25 0 5 10 15 20 25 5 10 15 2 0 2 5 0 5 10 1 5 2 0 2 5 Soil depths (cm) Figure 3. Number of individuals of the common species germinated from soil samples taken from different deptha 1992] ROCHADI ABDULHADI : Seed Banks in a Subtropical Forest D I S C U S S I O N It was anticipated that the germination technique used in this study should indicate both the density and diversity of seeds in the soil seed bank. But the technique may underestimate the numbers of seeds of certain spe- cies, particularly those species which are slow to germinate (Roberts, 1981). The present study sought to minimize these problems by extending the period of observation to 40 weeks and periodically disturbing the soil. Compared with other studies of seed banks in other rain forest soils, the number of species and seed densities found in the undisturbed forests in this study were comparable (Table 4). However, this number is lower than those in the secondary forest nearby (Abdulhadi & Lamb, 1987), even is so small compared with seed banks in Australian Savannah Woodland and Dry Sclerophyll Forest and in other forests in temperate regions. For example, Carrol and Ashton (1965) and Clifford and Mott (1986) found 2,772 — 25,589 seeds per m2 in both Queensland and Victoria. Likewise, in Co- nifer forests in U.S.A., Livingston & Allesio (1968) found 1289—5178 seeds per m2. From their review, Clifford & Mott (he. cit.) concluded that tropical soil have fewer germinable seeds in seed banks than temperate soils. The species and seed densities did not vary significantly in different seasons. The species composition was almost similar, with the Sorensen similarity values reaching up to of 78 %. Likewise, the similarity of the seed bank density at the different sampling times was comparatively high. Seasonal changes have been found in other forests, and Guevara and Gomez - Pompa (1972) attributed these to seed production by different species at different times of the year. Pulses in seed rain do occur in this forest (Abdulhadi, 1989). Despite such pulses the long lived and large soil seed pool of secondary trees, shrubs, herbs and vines apparently provide a buffer against such change and provide a high degree of constancy for the soil seed store. In the case of primary forest species these were only present in small numbers in the undisturbed forest soils. On the other hand, seed of primary forest species were common in the seed rain in this forest (Abdulhadi, 1989). This suggests the seed of these species is only present for a short period in the soil seed banks. The implication is that regeneration of these species under the forest canopy or in gaps is primarily recruited from recent seed rain rather than from the soil seed bank. The numbers of seeds in soil were significantly negatively correlated with the soil depths and only 25 percent of seeds were found below five centimetre soil depth. Similar observations have been reported elsewhere (Major & Pyott, 1966; Howard & Ashton, 1967 and Kellman, 1970). It has been suggested that seeds become burried by several mechanisms 10 REINWARDTIA [VOL. 11 such as being washed down through coarse-textured soil, or through worm and ant activities (Carrol & Ashton, 1965; McRill & Sagar, 1973 and Hopkins & Graham, 1983). These mechanisms were probably important in burying seeds in this undisturbed forest. In fact, most of the more common species found below 10 cm depth had small seeds. By contrast, shade tolerant species which tend to have larger seeds such as understorey shrubs and primary forest tree species, were restricted to the top 5 cm of soil. The extent to which small seeds enter the soil and move down the profile is probably determined in part by soil texture. Hopkins and Graham (1983) noted a higher proportion of seeds below 5 cm depth in a coarse- textured soil than in a fine-textured soil and attributed the difference to the ease with which seed could ebter the profiles. In most situations seed stored at the lower depth are ecologically un- important in that they are unlikely to be responsived to the usual dormancv- breaking environmental cues and are too deep for any seedling to emerge above ground. About the only situation in which such seed can become part of the plant community is when trees are uprooted and soil from the lower depth containing the seed is brought to the surface (Putz, 1983). However, Graham (pers. com.) found in North Queensland that a late secondary tree species, Aleurites moluccana, which has a large (up to 3 cm in maximum dimension) seed with a hard coat was able to germinate from seed stores below 15 cm in granitic, coarse-textured soil following a gap opening. Seed of this size must have been burried by surface soil movement and were presumably only able to germinate and reach the soil surface because of the large endosperm and food reserves and the coarse textures of the soil. In conclusion it seems that 1) the species richness and density of the soil seed bank in undisturbed sub-tropical rain forest were comparable to that found in many tropical rain forest soils. 2) The seed bank in undisturbed forest was relatively stable due to seed pools of large number of long lived, secondary species of grass, herbs, trees and vines, 3) The size of seed banks decreased with increasing soil depth. A K N O W L E D G M B N T S This study was financed by grants from the University of Queensland and the Australian International Assistance Bureau. I would like to thank Prof. H.T. Clifford and Dr. D. Lamb for help with identifications and for their helpful criticisms. 1992] ROCHADI ABDULHADI : Seed Banks in a Subtropical Forest 11 REFERENCES ABDULHADI, R. 1989. Sub-tropical rain forest seed dynamics. Ph.D Thesis, University of Queensland. ABDULHADI, R. & LAMB, D. 1937. Soil seed stores in a rainforest succession. In Kitching, R. (ed.) The ecology of Australia's wet tropics, pp 81—87. CARROL, E.J. & ASHTON, D. H. 1965. Seed storage in soils of several Victorian plant communities. Viet. Nat. 82, 102—110. CHEKE, A. S., NANAKARON, W. & YANKOSES, C. 1979. Dormancy and dispersal of seeds of secondarv forest species under canopy of a primary tropical rain forest in northern Thailand. Biotropica 11, 88—95. CLIFFORD, H. T. & MOTT, J. J. 1986. Regenerative process. In Clifford, H.T. and R.L. Specht (eds.) Tropical plant communities pp. 68—77. Department of Botany, University of Queensland. ENRIGHT, N. 1985. Existence of a soil seed bank under rain forest in New Guinea. Aust J. Ecol. 10, 67—71. GRAHAM, A. W. 1987. The buried viable seed bank of unlogged rain forest types in North Queensland M.Sc. Thesis, University of Queensland. GUEVARA, S. & GOMEZ—POMPA, A. 1972. Seeds from surface soils in tropical region of Vera Cruz, Mexico. J. Arn. Arbor. 53, 312—335. HALL, J.B. & SWAINE, M. D. 1980. Seed stocks in Ghanaian forest soils. Biotropica 12 (supl.), 8—15. HOPKINS, M.S. & GRAHAM, A.W. 1983. The species composition of soil seed banks beneath lowland tropical rain forests in North Queensland, Australia. Biotropica 15 (2), 9 0 - 99. HOWARD, T. & ASHTON, D.H. 1967. Studies of soil seed in snow gum woodland. Viet. Nat 84, 331—335. KEAY, R.W.J. 1960. Seeds in forest soils. Niger. For. Inf. Bull. 4, 1—12. KELLMAN, M.C. 1970. The viable seed content of some forest soils. J. Appl. Ecol. 11, 669—677. LAMB, D. 1980. Soil nitrogen mineralization in a secondary rain forest succession. Oecologia 47, 257—263. LIEW, T. C. 1973. Occurence of seeds in virgin forest top soil in Sabah. Malay. For. 36 (3), 185-193. LIVINGSTON, R.B. & ALLESSIO, M. L. 1968. Buried viable seed in successional field and forest stands, Harvard Massachusetts. Bull. Tor. Bot. Club 95, 58—69. MAJOR, J. & PYOTT, W.T. 1968. Buried viable seed in two California bunchgrass sites and their bearing on the definition of the flora. Vegetatio 13, 253—282. MCRILL, M.C. & S AGAR.G.R. 1973. Earthworms and seeds. Nature 243, 482. PUTZ, F. E. 1983. Treefall pits and mounds, buried seeds, and the importance of soil disturbance to pioneer trees on Barro Colorado Island, Panama. Ecology 64, 1069—1074. ROBERTS, H. A. 1981. Seed banks in soils. Adv. Appl. Biol. 6, 1—55. STEVENS, N. C. 1977. Geology and landforms. In Monroe, R and Stevens, N.C. (eds.) Border rangers, a land use conflict in regional perspective, pp. 1— 6. Royal Soc. of Queensland, Brisbane. SYMINGTON, C. F. 1933. The study of secondary growth on rain forest sites in Malaya. Malay. For. 2, 107—117. CONTENTS Page ROCHADI ABDULHADI Seed banks in a sub-tropical rain forest 1 ROCHADI ABDULHADI Floristic changes in a sub-tropical rain forest succession 13 A.J.G.H. KOSTERMANS Two remarkable Lindera species (Lauraceae) probably representing an undescribed genus 23 A.J.G.H. KOSTERMANS A new species of Diplodiscus Turcz. (Tiliaceae) related to Brownlowia Roxb 27 N. SASIDHARAN & K. SWARUPANANDAN A new species of Cassine (Celastraceae) from India , 29 A.J.G.H. KOSTERMANS Reinstatement of Pterocarpus echinata Pers. (Leguminosae — Papilionaceae) ., 33 JUMAAT H ADAM & GC. WlLCOCK. A new natural hybrid of Nepenthes from Mt. Kinabalu (Sabah) 35 A.J.G.H. KOSTERMANS Durio macrantha Kosterm. species nova (Bom- bacaceae) from North Sumatra 41 A.J.G.H. KOSTERMANS Salacia acuminatissima Kosterm., spec. nov. (Celastraceae) from Sri Lanka 53 A.J.G.H. KOSTERMANS Identity of Dracontomelum petelotii Tardleu -Blot (Anacard.) 55 Printed by c v. Bina Karya Cover Rein.Vol 11,Part 1, 1-55 11 Rein. Vol.11, Part 1, 1-55_Page_01 Rein. Vol.11, Part 1, 1-55_Page_02a Rein. Vol.11, Part 1, 1-55_Page_02b Rein. Vol.11, Part 1, 1-55_Page_03a Rein. Vol.11, Part 1, 1-55_Page_03b Rein. Vol.11, Part 1, 1-55_Page_04a Rein. Vol.11, Part 1, 1-55_Page_04b Rein. Vol.11, Part 1, 1-55_Page_05a Rein. Vol.11, Part 1, 1-55_Page_05b Rein. Vol.11, Part 1, 1-55_Page_06a Rein. Vol.11, Part 1, 1-55_Page_06b Rein. Vol.11, Part 1, 1-55_Page_29