- Email: [email protected]
Arbuscular mycorrhizal colonization of tree species grown in peat swamp forests of Central Kalimantan, Indonesia
Forest Ecology and Management 182 (2003) 381–386
Arbuscular mycorrhizal colonization of tree species grown in peat swamp forests of Central Kalimantan, Indonesia K. Tawarayaa,*, Y. Takayaa, M. Turjamanb, S.J. Tuahc, S.H. Liminc, Y. Tamaid, J.Y. Chae, T. Wagatsumaa, M. Osakid b
a Faculty of Agriculture, Yamagata University, Tsuruoka 997-8555, Japan Forest and Nature Conservation Research and Development Centre, Ministry of Forestry, Bogor 16610, Indonesia c Faculty of Agriculture, University of Palangka Raya, Palangka Raya 73112, Indonesia d Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan e Wakayama Experimental Forest, Field Science Center for Northern Biosphere, Hokkaido University, Kozakawa 649-4563, Japan
Received 11 December 2002; received in revised form 19 January 2003; accepted 4 February 2003
Abstract Arbuscular mycorrhizas improve the growth and nutrient uptake of plants and are formed in 80% of all land plants. Little information is available on the status of arbuscular mycorrhizas in tropical soils. The objective of this study was to clarify mycorrhizal colonization of tree species grown in tropical peat soils. Seedlings of 22 tree species in 14 families grown in a peat swamp forest of Central Kalimantan, Indonesia were collected in 2000 and 2001. Roots were stained with 0.05% aniline blue and arbuscules, vesicles and internal hyphae were observed under a compound microscope. Seventeen of 22 species showed arbuscular mycorrhizal colonization. Arbuscular mycorrhizal colonization was observed for the first time in roots of Shorea teysmanniana, Shorea balangeran, Shorea uliginosa (Dipterocarpaceae), Calophyllum sclerophyllum, Calophyllum soulattri (Guttiferae), Cratoxylum arborescens (Guttiferae), Tetramerista glabra (Tetrameristaceae), Palaquium gutta (Sapotaceae), Melastoma melabathricum (Melastomataceae), Gonystylus bancanus (Thymelaeaceae), Hevea brasiliensis (Euphorbiaceae) and Campnosperma auriculatum (Anacardiaceae). C. soulattri, C. arborescens, G. bancanus, Acacia mangium, M. melabathricum and H. brasiliensis showed a percentage mycorrhizal colonization of 50% or higher. No arbuscular mycorrhizal colonization was found in Hopea mengarawan (Dipterocarpaceae), Koompassia malacensis (Caesalpiniaceae), Tristaniopsis whiteana (Myrtaceae), Combretocapus rotundatus (Rhizophoraceae) and Dyera costulata (Apocynaceae). It is suggested that inoculation of arbuscular mycorrhizal fungi can improve the early growth of some tree species grown in peat swamp forests and this will be expected as a key technology to rehabilitate disturbed peatlands. # 2003 Elsevier Science B.V. All rights reserved. Keywords: Dipterocarpaceae; Kalimantan; Mycorrhiza; Peat swamp forest; Rehabilitation; Tropical soil
1. Introduction
*
Corresponding author. Tel.: þ81-235-28-2870; fax: þ81-235-25-8578. E-mail address: [email protected] (K. Tawaraya).
Tropical peat soils are distributed over Southeast Asia and form peat swamp forests. The tropical peat swamp forest is important as not only for its wealth of diverse bioresources but also its huge carbon pool.
0378-1127/$ – see front matter # 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0378-1127(03)00086-0
382
K. Tawaraya et al. / Forest Ecology and Management 182 (2003) 381–386
However, peat swamp forests have been decreasing due to conversion of forests into farm land by excessive draining, the use of shifting cultivation on a large scale, illegal logging and forest fire. It is necessary to understand edaphic factors, including the physical, chemical and biological properties of soil, in order to remediate disturbed forests. Of these properties, the biological is least known. Mycorrhizas affect the maintenance of vegetation in various ecosystems, and may play an important role in tropical peat swamp forests. Dipterocarpaceae plants which are the dominant tree species of tropical forests in Southeast Asia are known to form ectomycorrhiza on their roots. The ectomycorrhizal formation has been shown to increase the growth of Shorea macroptera (Turner et al., 1993), Hopea odorata and Hopea halferi (Yazid et al., 1994).
On the other hand, Afzelia, Alnus, Eucalyptus, Monopetalanthus, Populus, Salix, Tetraberlinia, Tristania and Uapaca form both arbuscular mycorrhiza and ectomycorrhiza. In Eucalyptus, the arbuscular mycorrhiza was formed in the early stage of growth, and ectomycorrhiza was formed in the late stage of the growth. For Eucalyptus an inoculation of both types of mycorrhizal fungi had more effect on growth promotion than with separate inoculations of either type of mycorrhizal fungi (Chen et al., 2000). Moyersoen et al. (2001) showed that arbuscular mycorrhizal colonization was about 40% in plants grown in heath forests and mixed Dipterocapaceae forest of Darussalam, Brunei. Arbuscular mycorrhiza may be formed even in trees, which grow in the peat swamp forest. It may be possible that arbuscular mycorrhiza improves the early growth of tree species
Table 1 Taxonomy of plant species collected from peat soils Order
Family
Species
Categorya
Ulticales
Moraceae
Ficus sp.
Tb
Theales
Dipterocarpaceae
H. mengarawan S. teysmanniana S. balangeran S. uliginosa C. sclerophyllum Calophyllum soulattri Calophyllum sp. C. arborescens
Ta Ta Ta Ta Ta Ta Ta Ta
Tetrameristaceae
T. glabra
Tb
Ebenales
Sapotaceae
P. gutta
N
Fabales
Caesalpiniaceae Mimosaceae
K. malacensis A. mangium
Ta Ta
Mytrales
Mytraceae Melastomataceae Thymelaeaceae
Syzygium sp. T. whiteana M. melabathricum G. bancanus
N Tb Tb, E Ta, Tp
Rhizophorales
Rhizophoraceae
C. rotundatus
Tb, E
Euphorbiales
Euphorbiaceae
H. brasiliensis
N
Sapindales
Anacardiaceae
C. auriculatum Mangifera sp.
Tb Tb
Gentianales
Apocynaceae
D. costulata
N
Guttiferae
a
Category: Ta, timbers actually exploited by logging companies; Tb, potentially exploitable timbers in the future or used by local populations for firewood or other domestic needs; Tp, totally protected tree species by Indonesian Law; N, tree species providing non-timber forest products such as fiber; fruits, nuts, bark, to local populations; E, early successional tree species.
K. Tawaraya et al. / Forest Ecology and Management 182 (2003) 381–386
and hence has an important role in the rehabilitation of disturbed peat swamp forests if mycorrhizal colonization in these soils is proven. In this study, we collected natural seedlings of representative tree species in peat soil of Central Kalimantan, Indonesia and investigated arbuscular mycorrhizal colonization in these plants in order to clarify the status of mycorrhiza in the tropical peat swamp forest.
2. Materials and methods 2.1. Sampling and identification of tree species This investigation focused on arbuscular mycorrhizal colonization of plant species grown in peat swamp forests. The study sites were located near Palangkaraya, Central Kalimantan, Indonesia. The mean daily temperature ranges from 24 to 30 8C and annual rainfall varies between 2500 to 2800 mm. Twenty-two species (20 genera) of representative trees were collected in September and October 2000 and November 2001 (Table 1). Tree species were grouped into five categories (Onguene and Kuyper, 2001). Most species are used as timber trees. Identification of tree species was done according to the morphological characteristics at the Forest and Nature Conservation Research and Development Centre, Ministry of Forestry, Bogor, Indonesia. Three replicate plant samples were collected from each of the 36 different sites. Roots were separated from shoots while in the field and packed into plastic bags and sent to the laboratory. 2.2. Determination of the mycorrhizal status Roots were washed with tap water to separate them from soil particles. The roots were cleared in KOH (100 g l1) for 1 h, acidified with diluted HCl (Phillips and Hayman, 1970) and stained with 500 mg l1 aniline blue for 15 min. The percentage mycorrhizal colonization was determined by the grid line intersect method (Giovannetti and Mosse, 1980) under a compound microscope (40–200). Presence of arbuscules, internal hyphae and vesicules was recorded from each intersect and expressed as a percentage of total root intersect. Some samples collected in 2000 were checked for ectomycorrhizal colonization.
383
3. Results Seventeen species out of 22 species showed mycorrhizal colonization (Tables 2 and 3). Arbuscular Table 2 Arbuscular mycorrhizal colonization of tree species collected in 2000 Species
Colonization (%)a
S. teysmanniana S. teysmanniana S. balangeran S. balangeran S. balangeran C. soulattri C. soulattri Calophyllum sp. C. arborescens T. glabra P. gutta Syzygium sp. Syzygium sp. Syzygium sp. T. whiteana G. bancanus G. bancanus C. rotundatus C. rotundatus H. brasiliensis C. auriculatum Mangifera sp.
10 9 14 0 3 41 60 4 69 15 17 9 20 7 0 58 15 0 0 47 28 6
a
5 8 1 0 3 26 14 3 4 7 3 1 5 2 0 11 2 0 0 2 7 4
Mean S:E:
Table 3 Arbuscular mycorrhizal colonization of tree species collected in 2001 Species
Colonization (%)a
Ficus sp. H. mengarawan S. balangeran S. uliginosa C. soulattri C. sclerophyllum P. gutta Koompassia malaccensis A. mangium M. melabathricum G. bancanus G. bancanus H. brasiliensis D. costulata
15 0 10 17 0 18 0 0 65 56 0 0 72 0
a
Mean S:E:
9 0 10 6 0 13 0 0 4 9 0 0 2 0
384
K. Tawaraya et al. / Forest Ecology and Management 182 (2003) 381–386
Fig. 1. Arbuscular mycorrhizal colonization in root of S. teysmanniana (A), S. balangeran (B), G. bancanus (C) and H. brasiliensis (D).
mycorrhizal colonization was observed for the first time in roots of Shorea teysmanniana, S. balangeran, Shorea uliginosa (Dipterocarpaceae), Calophyllum sclerophyllum, C. soulattri, C. arborescens (Guttiferae), Tetramerista glabra (Tetrameristaceae), Palaquium gutta (Sapotaceae), Melastoma melabathricum (Melastomataceae), Gonystylus bancanus (Thymelaeaceae), Hevea brasiliensis (Euphorbiaceae) and Campnosperma auriculatum (Anacardiaceae). C. soulattri, C. arborescens, G. bancanus, Acacia mangium, M. melabathricum and H. brasiliensis showed a percentage mycorrhizal colonization of 50% or higher. Arbuscular mycorrhizal colonization of S. teysmanniana and S. balangeran was not so high and clear vesicle formation was localized (Fig. 1A and B). S. teysmanniana and S. balangeran were also colonized with ectomycorrhizal fungi. Many vesicles were formed in the roots of G. bancanus and H. brasiliensis (Fig. 1C and D). No arbuscular mycorrhizal colonization was found in Hopea mengarawan (Dipterocarpaceae), Koompassia malacensis (Caesalpiniaceae), Tristaniopsis whiteana (Myrtaceae), Combretocapus rotundatus (Rhizophoraceae) and Dyera costulata (Apocynaceae).
4. Discussion Arbuscular mycorrhizal colonization was observed in 77% of these plant samples from tropical peat swamp forest of Central Kalimantan and in 17 tree species colonization was observed for the first time. Arbuscular mycorrhizal colonization has never been reported in any species of Dipterocarpaceae and Tetrameristaceae. In tropical forests other than peat swamp forests, arbuscular mycorrhizal colonization was shown to be present in heath forests (Moyersoen et al., 2001), dipterocarp forests and secondary forests (Metcalfe et al., 1998), monodominant lowland and upland forests (Torti et al., 1997) and lowland rainforests (Bakarr and Janos, 1996). In temperate aquatic conditions, arbuscular mycorrhiza was also observed in fens (Cornwell et al., 2001). Dipterocarpaceae is one of the most important families in peat swamp forests. It is well known that ectomycorrhiza is formed in the roots of Dipterocarpaceae (Louis, 1988; Turner et al., 1993; Yazid et al., 1994). Early growth of some Dipterocarpaceae was improved with the inoculation of ectomycorrhizal fungi (Yazid et al., 1994). However, until now, there
K. Tawaraya et al. / Forest Ecology and Management 182 (2003) 381–386
has been no report on arbuscular mycorrhizal colonization in Dipterocarpaceae. Arbuscular mycorrhizal colonization was observed in three species of Shorea in Dipterocarpaceae. These three Shorea are valuable timber species and their populations have been decreasing in Indonesia due to illegal logging. Soil nutrient availability is one of the limiting factors for the early growth of transplanted seedlings in peat swamp forests. Inoculation of arbuscular mycorrhizal fungi may improve the early growth of these species. Ectomycorrhizal colonization was also observed in two of the above Shorea spp. It is also possible that dual inoculation of ectomycorrhizal fungi and arbuscular mycorrhizal fungi improve the early growth synergistically as already shown in Eucalyptus (Chen et al., 2000). It is necessary to investigate arbuscular mycorrhizal colonization in other Dipterocarpaceae species as there are more than 470 species, 13 genera in Dipterocapaceae (Smits, 1994). Our results of arbuscular mycorrhizal colonization in some genera are consistent with previous reports of Smits (1992) with Ficus sp., Callophyllum sp., Palaquium sp. and Syzygium sp. in East Kalimantan and of Moyersoen et al. (2001) with Callophyllum ferugineum, Syzygium bankensis, Tristania beccarii in Darussalam, Brunei. There are also reports on arbuscular mycorrhizal colonization in other species of Anacardiaceae, Euphorbiaceae, Mimosaceae and Sapotaceae in Cameroon (Onguene and Kuyper, 2001) and Guttiferae and Mytraceae in Darssalam, Brunei (Moyersoen et al., 2001) and Mimosaceae in Uruguay (Frioni et al., 1999) and in Sierra Leone (Bakarr and Janos, 1996). Arbuscular mycorrhizal colonization in A. mangium has been previously reported in Sierra Leone (Bakarr and Janos, 1996). Growth of this species has been shown to improve with the inoculation of mycorrhizal fungi (Habte and Soedarjo, 1995). Along with Dipterocapaceae, these species are also important in Central Kalimantan. It is possible that the early growth of these species in tropical peat soil can also be improved with the inoculations of the arbuscular mycorrhizal fungi. We have carried out a trap culture with peat soils and isolated some Glomus spp. and Entrophospora spp. Effects of these isolates on the growth of seedlings will be clarified if seeds of native species in peat swamp forests are obtained.
385
The seedlings collected during this experiment were 30 cm or less in height and seemed to be less than a few years old. Older seedlings may also be included, because the light environment in the collecting site was not completely consistent. Therefore, it is also necessary to examine the mycorrhiza colonization of younger seedlings (1-year old or younger). Since the flowering and fruiting of the trees which grow in peat swamp forests is not well understood, it is difficult to obtain the seeds. Therefore, the ageing variation in mycorrhizal colonization of these tree species by pot experiment using seeds has not yet been examined. It is possible to observe mycorrhizal colonization in trees only several months old, if the procurement of seeds becomes less difficult.
Acknowledgements This research was supported in part by the Core University Program of Japan Society for the Promotion of Science, Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (No. 13375011) and the Toyota Foundation. We are grateful to members of Centre for International Cooperation in Management of Tropical Peatland (CIMTROP), University of Palangka Raya for field support. References Bakarr, M.I., Janos, D.P., 1996. Mycorrhizal associations of tropical legume trees in Sierra Leone, West Africa. For. Ecol. Manage. 89, 89–92. Chen, Y.L., Brundrett, M.C., Dell, B., 2000. Effects of ectomycorrhizas and vesicular-arbuscular mycorrhizas, alone or in competition, on root colonization and growth of Eucalyptus globulus and E. urophylla. New Phytol. 146, 545–556. Cornwell, W.K., Bedford, B.L., Chapin, C.T., 2001. Occurrence of arbuscular mycorrhizal fungi in a phosphorus-poor wetland and mycorrhizal response to phosphorus fertilization. Am. J. Bot. 88, 1824–1829. Frioni, L., Minasian, H., Volfovicz, R., 1999. Arbuscular mycorrhizae and ectomycorrhizae in native tree legumes in Uruguay. For. Ecol. Manage. 115, 41–47. Giovannetti, M., Mosse, B., 1980. An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol. 84, 489–500. Habte, M., Soedarjo, M., 1995. Mycorrhizal inoculation effect in Acacia mangium grown in an acid oxisol amended with gypsum. J. Plant Nutr. 18, 2059–2073.
386
K. Tawaraya et al. / Forest Ecology and Management 182 (2003) 381–386
Louis, I., 1988. Ecto- and ectendomycorrhizae in the tropical Dipterocarp, Shorea parvifolia. Mycologia 80, 845–849. Metcalfe, D.J., Grubb, P.J., Turner, I.M., 1998. The ecology of very small-seeded shade-tolerant trees and shrubs in lowland rain forest in Singapore. Plant Ecol. 134, 131–149. Moyersoen, B., Becker, P., Alexander, I.J., 2001. Are ectomycorrhizas more abundant than arbuscular mycorrhizas in tropical heath forests? New Phytol. 150, 591–599. Onguene, N.A., Kuyper, T.W., 2001. Mycorrhizal associations in the rain forest of South Cameroon. For. Ecol. Manage. 140, 277–287. Phillips, J.M., Hayman, D.S., 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55, 158–161.
Smits, W.T.M., 1992. Mycorrhizal studies in Dipterocarp forest in Indonesia. In: Alexander, I.J. (Ed.), Mycorrhizas in Ecosystems. CAB International, Wallingford, pp. 283–292. Smits, W.T.M., 1994. Dipterocarpaceae: Mycorrhizae and Regeneration. Backhuys Publishers, AH Leiden, The Netherlands. Torti, S.D., Coley, P.D., Janos, D.P., 1997. Vesicular-arbuscular mycorrhizae in two tropical monodominant trees. J. Trop. Ecol. 13, 623–629. Turner, I.M., Brown, N.D., Newton, A.C., 1993. The effect of fertilizer application on dipterocarp seedling growth and mycorrhizal infection. For. Ecol. Manage. 57, 329–337. Yazid, S.M., Lee, S.S., Lapeyrie, F., 1994. Growth stimulation of Hopea spp. (Dipterocarpaceae) seedlings following ectomycorrhizal inoculation with an exotic strain of Pisolithus tinctorius. For. Ecol. Manage. 67, 339–343.
Arbuscular mycorrhizal colonization of tree species grown in peat swamp forests of Central Kalimantan, Indonesia K. Tawarayaa,*, Y. Takayaa, M. Turjamanb, S.J. Tuahc, S.H. Liminc, Y. Tamaid, J.Y. Chae, T. Wagatsumaa, M. Osakid b
a Faculty of Agriculture, Yamagata University, Tsuruoka 997-8555, Japan Forest and Nature Conservation Research and Development Centre, Ministry of Forestry, Bogor 16610, Indonesia c Faculty of Agriculture, University of Palangka Raya, Palangka Raya 73112, Indonesia d Graduate School of Agriculture, Hokkaido University, Sapporo 060-8589, Japan e Wakayama Experimental Forest, Field Science Center for Northern Biosphere, Hokkaido University, Kozakawa 649-4563, Japan
Received 11 December 2002; received in revised form 19 January 2003; accepted 4 February 2003
Abstract Arbuscular mycorrhizas improve the growth and nutrient uptake of plants and are formed in 80% of all land plants. Little information is available on the status of arbuscular mycorrhizas in tropical soils. The objective of this study was to clarify mycorrhizal colonization of tree species grown in tropical peat soils. Seedlings of 22 tree species in 14 families grown in a peat swamp forest of Central Kalimantan, Indonesia were collected in 2000 and 2001. Roots were stained with 0.05% aniline blue and arbuscules, vesicles and internal hyphae were observed under a compound microscope. Seventeen of 22 species showed arbuscular mycorrhizal colonization. Arbuscular mycorrhizal colonization was observed for the first time in roots of Shorea teysmanniana, Shorea balangeran, Shorea uliginosa (Dipterocarpaceae), Calophyllum sclerophyllum, Calophyllum soulattri (Guttiferae), Cratoxylum arborescens (Guttiferae), Tetramerista glabra (Tetrameristaceae), Palaquium gutta (Sapotaceae), Melastoma melabathricum (Melastomataceae), Gonystylus bancanus (Thymelaeaceae), Hevea brasiliensis (Euphorbiaceae) and Campnosperma auriculatum (Anacardiaceae). C. soulattri, C. arborescens, G. bancanus, Acacia mangium, M. melabathricum and H. brasiliensis showed a percentage mycorrhizal colonization of 50% or higher. No arbuscular mycorrhizal colonization was found in Hopea mengarawan (Dipterocarpaceae), Koompassia malacensis (Caesalpiniaceae), Tristaniopsis whiteana (Myrtaceae), Combretocapus rotundatus (Rhizophoraceae) and Dyera costulata (Apocynaceae). It is suggested that inoculation of arbuscular mycorrhizal fungi can improve the early growth of some tree species grown in peat swamp forests and this will be expected as a key technology to rehabilitate disturbed peatlands. # 2003 Elsevier Science B.V. All rights reserved. Keywords: Dipterocarpaceae; Kalimantan; Mycorrhiza; Peat swamp forest; Rehabilitation; Tropical soil
1. Introduction
*
Corresponding author. Tel.: þ81-235-28-2870; fax: þ81-235-25-8578. E-mail address: [email protected] (K. Tawaraya).
Tropical peat soils are distributed over Southeast Asia and form peat swamp forests. The tropical peat swamp forest is important as not only for its wealth of diverse bioresources but also its huge carbon pool.
0378-1127/$ – see front matter # 2003 Elsevier Science B.V. All rights reserved. doi:10.1016/S0378-1127(03)00086-0
382
K. Tawaraya et al. / Forest Ecology and Management 182 (2003) 381–386
However, peat swamp forests have been decreasing due to conversion of forests into farm land by excessive draining, the use of shifting cultivation on a large scale, illegal logging and forest fire. It is necessary to understand edaphic factors, including the physical, chemical and biological properties of soil, in order to remediate disturbed forests. Of these properties, the biological is least known. Mycorrhizas affect the maintenance of vegetation in various ecosystems, and may play an important role in tropical peat swamp forests. Dipterocarpaceae plants which are the dominant tree species of tropical forests in Southeast Asia are known to form ectomycorrhiza on their roots. The ectomycorrhizal formation has been shown to increase the growth of Shorea macroptera (Turner et al., 1993), Hopea odorata and Hopea halferi (Yazid et al., 1994).
On the other hand, Afzelia, Alnus, Eucalyptus, Monopetalanthus, Populus, Salix, Tetraberlinia, Tristania and Uapaca form both arbuscular mycorrhiza and ectomycorrhiza. In Eucalyptus, the arbuscular mycorrhiza was formed in the early stage of growth, and ectomycorrhiza was formed in the late stage of the growth. For Eucalyptus an inoculation of both types of mycorrhizal fungi had more effect on growth promotion than with separate inoculations of either type of mycorrhizal fungi (Chen et al., 2000). Moyersoen et al. (2001) showed that arbuscular mycorrhizal colonization was about 40% in plants grown in heath forests and mixed Dipterocapaceae forest of Darussalam, Brunei. Arbuscular mycorrhiza may be formed even in trees, which grow in the peat swamp forest. It may be possible that arbuscular mycorrhiza improves the early growth of tree species
Table 1 Taxonomy of plant species collected from peat soils Order
Family
Species
Categorya
Ulticales
Moraceae
Ficus sp.
Tb
Theales
Dipterocarpaceae
H. mengarawan S. teysmanniana S. balangeran S. uliginosa C. sclerophyllum Calophyllum soulattri Calophyllum sp. C. arborescens
Ta Ta Ta Ta Ta Ta Ta Ta
Tetrameristaceae
T. glabra
Tb
Ebenales
Sapotaceae
P. gutta
N
Fabales
Caesalpiniaceae Mimosaceae
K. malacensis A. mangium
Ta Ta
Mytrales
Mytraceae Melastomataceae Thymelaeaceae
Syzygium sp. T. whiteana M. melabathricum G. bancanus
N Tb Tb, E Ta, Tp
Rhizophorales
Rhizophoraceae
C. rotundatus
Tb, E
Euphorbiales
Euphorbiaceae
H. brasiliensis
N
Sapindales
Anacardiaceae
C. auriculatum Mangifera sp.
Tb Tb
Gentianales
Apocynaceae
D. costulata
N
Guttiferae
a
Category: Ta, timbers actually exploited by logging companies; Tb, potentially exploitable timbers in the future or used by local populations for firewood or other domestic needs; Tp, totally protected tree species by Indonesian Law; N, tree species providing non-timber forest products such as fiber; fruits, nuts, bark, to local populations; E, early successional tree species.
K. Tawaraya et al. / Forest Ecology and Management 182 (2003) 381–386
and hence has an important role in the rehabilitation of disturbed peat swamp forests if mycorrhizal colonization in these soils is proven. In this study, we collected natural seedlings of representative tree species in peat soil of Central Kalimantan, Indonesia and investigated arbuscular mycorrhizal colonization in these plants in order to clarify the status of mycorrhiza in the tropical peat swamp forest.
2. Materials and methods 2.1. Sampling and identification of tree species This investigation focused on arbuscular mycorrhizal colonization of plant species grown in peat swamp forests. The study sites were located near Palangkaraya, Central Kalimantan, Indonesia. The mean daily temperature ranges from 24 to 30 8C and annual rainfall varies between 2500 to 2800 mm. Twenty-two species (20 genera) of representative trees were collected in September and October 2000 and November 2001 (Table 1). Tree species were grouped into five categories (Onguene and Kuyper, 2001). Most species are used as timber trees. Identification of tree species was done according to the morphological characteristics at the Forest and Nature Conservation Research and Development Centre, Ministry of Forestry, Bogor, Indonesia. Three replicate plant samples were collected from each of the 36 different sites. Roots were separated from shoots while in the field and packed into plastic bags and sent to the laboratory. 2.2. Determination of the mycorrhizal status Roots were washed with tap water to separate them from soil particles. The roots were cleared in KOH (100 g l1) for 1 h, acidified with diluted HCl (Phillips and Hayman, 1970) and stained with 500 mg l1 aniline blue for 15 min. The percentage mycorrhizal colonization was determined by the grid line intersect method (Giovannetti and Mosse, 1980) under a compound microscope (40–200). Presence of arbuscules, internal hyphae and vesicules was recorded from each intersect and expressed as a percentage of total root intersect. Some samples collected in 2000 were checked for ectomycorrhizal colonization.
383
3. Results Seventeen species out of 22 species showed mycorrhizal colonization (Tables 2 and 3). Arbuscular Table 2 Arbuscular mycorrhizal colonization of tree species collected in 2000 Species
Colonization (%)a
S. teysmanniana S. teysmanniana S. balangeran S. balangeran S. balangeran C. soulattri C. soulattri Calophyllum sp. C. arborescens T. glabra P. gutta Syzygium sp. Syzygium sp. Syzygium sp. T. whiteana G. bancanus G. bancanus C. rotundatus C. rotundatus H. brasiliensis C. auriculatum Mangifera sp.
10 9 14 0 3 41 60 4 69 15 17 9 20 7 0 58 15 0 0 47 28 6
a
5 8 1 0 3 26 14 3 4 7 3 1 5 2 0 11 2 0 0 2 7 4
Mean S:E:
Table 3 Arbuscular mycorrhizal colonization of tree species collected in 2001 Species
Colonization (%)a
Ficus sp. H. mengarawan S. balangeran S. uliginosa C. soulattri C. sclerophyllum P. gutta Koompassia malaccensis A. mangium M. melabathricum G. bancanus G. bancanus H. brasiliensis D. costulata
15 0 10 17 0 18 0 0 65 56 0 0 72 0
a
Mean S:E:
9 0 10 6 0 13 0 0 4 9 0 0 2 0
384
K. Tawaraya et al. / Forest Ecology and Management 182 (2003) 381–386
Fig. 1. Arbuscular mycorrhizal colonization in root of S. teysmanniana (A), S. balangeran (B), G. bancanus (C) and H. brasiliensis (D).
mycorrhizal colonization was observed for the first time in roots of Shorea teysmanniana, S. balangeran, Shorea uliginosa (Dipterocarpaceae), Calophyllum sclerophyllum, C. soulattri, C. arborescens (Guttiferae), Tetramerista glabra (Tetrameristaceae), Palaquium gutta (Sapotaceae), Melastoma melabathricum (Melastomataceae), Gonystylus bancanus (Thymelaeaceae), Hevea brasiliensis (Euphorbiaceae) and Campnosperma auriculatum (Anacardiaceae). C. soulattri, C. arborescens, G. bancanus, Acacia mangium, M. melabathricum and H. brasiliensis showed a percentage mycorrhizal colonization of 50% or higher. Arbuscular mycorrhizal colonization of S. teysmanniana and S. balangeran was not so high and clear vesicle formation was localized (Fig. 1A and B). S. teysmanniana and S. balangeran were also colonized with ectomycorrhizal fungi. Many vesicles were formed in the roots of G. bancanus and H. brasiliensis (Fig. 1C and D). No arbuscular mycorrhizal colonization was found in Hopea mengarawan (Dipterocarpaceae), Koompassia malacensis (Caesalpiniaceae), Tristaniopsis whiteana (Myrtaceae), Combretocapus rotundatus (Rhizophoraceae) and Dyera costulata (Apocynaceae).
4. Discussion Arbuscular mycorrhizal colonization was observed in 77% of these plant samples from tropical peat swamp forest of Central Kalimantan and in 17 tree species colonization was observed for the first time. Arbuscular mycorrhizal colonization has never been reported in any species of Dipterocarpaceae and Tetrameristaceae. In tropical forests other than peat swamp forests, arbuscular mycorrhizal colonization was shown to be present in heath forests (Moyersoen et al., 2001), dipterocarp forests and secondary forests (Metcalfe et al., 1998), monodominant lowland and upland forests (Torti et al., 1997) and lowland rainforests (Bakarr and Janos, 1996). In temperate aquatic conditions, arbuscular mycorrhiza was also observed in fens (Cornwell et al., 2001). Dipterocarpaceae is one of the most important families in peat swamp forests. It is well known that ectomycorrhiza is formed in the roots of Dipterocarpaceae (Louis, 1988; Turner et al., 1993; Yazid et al., 1994). Early growth of some Dipterocarpaceae was improved with the inoculation of ectomycorrhizal fungi (Yazid et al., 1994). However, until now, there
K. Tawaraya et al. / Forest Ecology and Management 182 (2003) 381–386
has been no report on arbuscular mycorrhizal colonization in Dipterocarpaceae. Arbuscular mycorrhizal colonization was observed in three species of Shorea in Dipterocarpaceae. These three Shorea are valuable timber species and their populations have been decreasing in Indonesia due to illegal logging. Soil nutrient availability is one of the limiting factors for the early growth of transplanted seedlings in peat swamp forests. Inoculation of arbuscular mycorrhizal fungi may improve the early growth of these species. Ectomycorrhizal colonization was also observed in two of the above Shorea spp. It is also possible that dual inoculation of ectomycorrhizal fungi and arbuscular mycorrhizal fungi improve the early growth synergistically as already shown in Eucalyptus (Chen et al., 2000). It is necessary to investigate arbuscular mycorrhizal colonization in other Dipterocarpaceae species as there are more than 470 species, 13 genera in Dipterocapaceae (Smits, 1994). Our results of arbuscular mycorrhizal colonization in some genera are consistent with previous reports of Smits (1992) with Ficus sp., Callophyllum sp., Palaquium sp. and Syzygium sp. in East Kalimantan and of Moyersoen et al. (2001) with Callophyllum ferugineum, Syzygium bankensis, Tristania beccarii in Darussalam, Brunei. There are also reports on arbuscular mycorrhizal colonization in other species of Anacardiaceae, Euphorbiaceae, Mimosaceae and Sapotaceae in Cameroon (Onguene and Kuyper, 2001) and Guttiferae and Mytraceae in Darssalam, Brunei (Moyersoen et al., 2001) and Mimosaceae in Uruguay (Frioni et al., 1999) and in Sierra Leone (Bakarr and Janos, 1996). Arbuscular mycorrhizal colonization in A. mangium has been previously reported in Sierra Leone (Bakarr and Janos, 1996). Growth of this species has been shown to improve with the inoculation of mycorrhizal fungi (Habte and Soedarjo, 1995). Along with Dipterocapaceae, these species are also important in Central Kalimantan. It is possible that the early growth of these species in tropical peat soil can also be improved with the inoculations of the arbuscular mycorrhizal fungi. We have carried out a trap culture with peat soils and isolated some Glomus spp. and Entrophospora spp. Effects of these isolates on the growth of seedlings will be clarified if seeds of native species in peat swamp forests are obtained.
385
The seedlings collected during this experiment were 30 cm or less in height and seemed to be less than a few years old. Older seedlings may also be included, because the light environment in the collecting site was not completely consistent. Therefore, it is also necessary to examine the mycorrhiza colonization of younger seedlings (1-year old or younger). Since the flowering and fruiting of the trees which grow in peat swamp forests is not well understood, it is difficult to obtain the seeds. Therefore, the ageing variation in mycorrhizal colonization of these tree species by pot experiment using seeds has not yet been examined. It is possible to observe mycorrhizal colonization in trees only several months old, if the procurement of seeds becomes less difficult.
Acknowledgements This research was supported in part by the Core University Program of Japan Society for the Promotion of Science, Grant-in-Aid for Scientific Research from the Ministry of Education, Culture, Sports, Science and Technology of Japan (No. 13375011) and the Toyota Foundation. We are grateful to members of Centre for International Cooperation in Management of Tropical Peatland (CIMTROP), University of Palangka Raya for field support. References Bakarr, M.I., Janos, D.P., 1996. Mycorrhizal associations of tropical legume trees in Sierra Leone, West Africa. For. Ecol. Manage. 89, 89–92. Chen, Y.L., Brundrett, M.C., Dell, B., 2000. Effects of ectomycorrhizas and vesicular-arbuscular mycorrhizas, alone or in competition, on root colonization and growth of Eucalyptus globulus and E. urophylla. New Phytol. 146, 545–556. Cornwell, W.K., Bedford, B.L., Chapin, C.T., 2001. Occurrence of arbuscular mycorrhizal fungi in a phosphorus-poor wetland and mycorrhizal response to phosphorus fertilization. Am. J. Bot. 88, 1824–1829. Frioni, L., Minasian, H., Volfovicz, R., 1999. Arbuscular mycorrhizae and ectomycorrhizae in native tree legumes in Uruguay. For. Ecol. Manage. 115, 41–47. Giovannetti, M., Mosse, B., 1980. An evaluation of techniques for measuring vesicular-arbuscular mycorrhizal infection in roots. New Phytol. 84, 489–500. Habte, M., Soedarjo, M., 1995. Mycorrhizal inoculation effect in Acacia mangium grown in an acid oxisol amended with gypsum. J. Plant Nutr. 18, 2059–2073.
386
K. Tawaraya et al. / Forest Ecology and Management 182 (2003) 381–386
Louis, I., 1988. Ecto- and ectendomycorrhizae in the tropical Dipterocarp, Shorea parvifolia. Mycologia 80, 845–849. Metcalfe, D.J., Grubb, P.J., Turner, I.M., 1998. The ecology of very small-seeded shade-tolerant trees and shrubs in lowland rain forest in Singapore. Plant Ecol. 134, 131–149. Moyersoen, B., Becker, P., Alexander, I.J., 2001. Are ectomycorrhizas more abundant than arbuscular mycorrhizas in tropical heath forests? New Phytol. 150, 591–599. Onguene, N.A., Kuyper, T.W., 2001. Mycorrhizal associations in the rain forest of South Cameroon. For. Ecol. Manage. 140, 277–287. Phillips, J.M., Hayman, D.S., 1970. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc. 55, 158–161.
Smits, W.T.M., 1992. Mycorrhizal studies in Dipterocarp forest in Indonesia. In: Alexander, I.J. (Ed.), Mycorrhizas in Ecosystems. CAB International, Wallingford, pp. 283–292. Smits, W.T.M., 1994. Dipterocarpaceae: Mycorrhizae and Regeneration. Backhuys Publishers, AH Leiden, The Netherlands. Torti, S.D., Coley, P.D., Janos, D.P., 1997. Vesicular-arbuscular mycorrhizae in two tropical monodominant trees. J. Trop. Ecol. 13, 623–629. Turner, I.M., Brown, N.D., Newton, A.C., 1993. The effect of fertilizer application on dipterocarp seedling growth and mycorrhizal infection. For. Ecol. Manage. 57, 329–337. Yazid, S.M., Lee, S.S., Lapeyrie, F., 1994. Growth stimulation of Hopea spp. (Dipterocarpaceae) seedlings following ectomycorrhizal inoculation with an exotic strain of Pisolithus tinctorius. For. Ecol. Manage. 67, 339–343.