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The effect of fertilizer application on dipterocarp seedling growth and mycorrhizal infection
Forest Ecology and Management, 57 ( 1993 ) 329-337
329
Elsevier Science Publishers B.V., Amsterdam
Short Communication
The effect of fertilizer application on dipterocarp seedling growth and mycorrhizal infection I.M. Turnera, N.D.
Brown b and A.C. Newton c
aDepartment of Botany, National University of Singapore, Lower Kent Ridge Road, Singapore 0511. Singapore bOxford Forestry Institute, University of Oxford, South Parks Road, Oxford OX1 3RB, UK Clnstitute of Terrestrial Ecology, Bush Estate, Penicuik, Ett26 OQB, UK (Accepted 13 August 1992)
ABSTRACT Turner, I.M., Brown, N.D. and Newton, A.C., 1993. The effect of fertilizer application on dipterocarp seedling growth and mycorrhizal infection. For.Ecol. Manage., 57: 329-337. In three independent experiments, application of fertilizers had no effect on the growth of dipterocarp seedlings. The experiments involved application of: ( 1 ) NPK at a rate of 10 g m -2 N, P205 and K20 to Shorea macroptera Dyer seedlings grown in pots of forest soil under nursery conditions in Penang, Malaysia; (2) N at a rate of 10 g m -2 and/or P at a rate of 5 g m -2 in a factorial design to 8month-old Shorea curtisii Dyer ex King seedlings growing wild in coastal hill dipterocarp forest in Penang, Malaysia; (3) NKP at a rate of 10 g m -2 three times over 10 months to Hopea beccariana Burck seedlings growing wild in lowland mixed dipterocarp forest in Sahah, Malaysia. In Experiment 1, fertilizer application significantly increased the extent of ectomycorrhizal (ECM) infection of the S. macroptera roots, and unfertilized seedlings showed a closer correlation between extent of ECM infection and growth than fertilized seedlings. These preliminary results suggest that dipterocarp seedlings may only be responsive to fertilizer addition when grown at very low nutrient availabilities, and that ECM infection may be of great importance to seedling growth under such conditions.
INTRODUCTION
The Dipterocarpaceae dominate the canopy of the lowland tropical rain forests of the Malay Peninsula, Sumatra, Borneo and the Philippines (Whitmore, 1989) and they currently supply over half of the World's hardwood (Ashton, 1989). Detailed information on the influence of environmental conditions on the growth and survival of juvenile dipterocarps is required, Correspondence to: I.M. Turner, Department of Botany, National University of Singapore, Lower Kent Ridge Road, Singapore 051 I. Fax, Singapore 779 5671.
© 1993 Elsevier Science Publishers B.V. All rights reserved 0378-1127/93/$06.00
330
I.M. TURNER ETAL.
particularly for the commercially most important groups such as the red meranti Shorea species. Little work has been carried out on the responses of dipterocarp seedlings to soil nutrient status. Dipterocarps have ectomycorrhizal (ECM) associations (Singh, 1966; Lee, 1990) which may be obligate for normal growth (Smits, 1985). ECM symbioses have been postulated to be the key to the dominance of the Dipterocarpaceae in Southeast Asia (Connell and Lowman, 1989). This paper presents the results of some preliminary experiments investigating the influence of fertilizer application on seedling growth in the nursery and in the forest. In one experiment the extent of ECM infection of the seedlings was assessed and related to fertilizer treatment. METHODS
Experiment 1 Forty seedlings of Shorea macroptera Dyer were grown from locally collected seed in polyethylene pots of sieved forest topsoil (about 1.5 1) under the shade of a large Eugenia grandis Wight tree at Muka Head Field Station, Penang, Malaysia. The seeds and soil were collected from under mature dipterocarps in the adjacent Pantai Acheh Forest Reserve. The soils of the Reserve are Typic Paleudults (Siew, 1969), a group which generally has moderate to low fertility in Peninsular Malaysia (Soong and Lau, 1977 ). At the start of the experiment half of the eight-month-old seedlings were randomly selected and given a fertilizer treatment of 10 g m-2 of combined N, P205 and KaO in the form of a proprietary N P K fertilizer (Wonder-Gro, The Agricultural Farming Co., Penang, Malaysia) in solution (equivalent to 100 mg of each of N, P and K per pot). Six months later, all the plants were harvested, dried in an 80°C oven for 2 days and weighed. Small samples (about ten 2-cm pieces of lateral root with their attached side-branches) of the root system of each S. macroptera seedling were taken during the harvesting and fixed in formyl acetic alcohol for subsequent analysis of ECM infection. Each sample was examined, immersed in water, under a × 6 - X 45 zoom objective. A series of randomly selected fields was assessed, until a total of more than 200 tips per sample had been counted. Infection was characterized by the presence of a complete fungal mantle on the root tip. The extent of infection was expressed as the percentage of root tips that were mycorrhizal, with the tips of branching mycorrhizas being counted separately.
Experiment 2 A population of Shorea curtisii Dyer ex King seedlings originating from natural regeneration, approximately eight months old at the start of the ex-
FERTILIZER EFFECTS ON DIPTEROCARPS
331
periment, was located in Pantai Acheh Forest Reserve, Penang, Malaysia, in a coastal hill dipterocarp forest (Turner, 1989). Eight 1 m × 1 m plots were laid out in the area, which was near a small canopy opening. Three fertilizer treatments were randomly assigned to the plots: NHaNO3 applied at a rate of 10 g m - 2 N, P205 applied at a rate of 5 g m - 2 p and a combined application of N and P at the above rates plus an unfertilized control. All treatments were replicated twice. All the seedlings, ranging from 17 to 46 per plot, were tagged, then heights and basal stem diameters were measured using vernier callipers. Fertilizer was applied dry, by the hand, to the surface of the soil in each plot. All the seedlings were remeasured after 5 months.
Experiment 3 One hundred wild Hopea beccariana Burck seedlings ranging from 130 m m to 1030 m m in height were tagged and measured in two 6-m 2 plots located under the closed canopy of primary lowland dipterocarp rain forest in the D a n u m Valley Conservation Area, Sabah, Malaysia. The two plots were aligned down a gentle slope (less than 3 ° ) and were separated by a distance of 1 m. The upslope plot had a canopy openness value (proportion of total sky unobscured by forest canopy) of 4.7% as determined from a vertical hemispherical photograph taken at the start of the experiment. The downslope plot had 2.5% canopy openness and was treated with 10 g m -2 of N P K fertilizer (Rustica 15:15:6:4, Ruhr-Stickstoff AG, Germany), broadcast evenly in dry pellet form at the start of the experiment. Further fertilizer applications were made at the same dosage 2.5 and 5 months later, at which time all the seedlings on both plots were remeasured for height. All seedlings were measured for a final time 10 months after the start of the experiment. RESULTS
Experiment I The mean (_+standard error) of the total dry mass of the fertilized and unfertilized groups of S. macroptera seedlings were 10.4 (_+0.8)g and 9.2 TABLE 1 T h e relationship between the extent o f m y c o r r h i z a l infection a n d growth o f pot-grown S. macroptera seedlings ( E x p e r i m e n t 1 ). S p e a r m a n ' s rank correlation coefficient
Total dry weight Root:shoot ratio
All seedlings n=401
Control group n=201
Fertilized group n=20 t
0.555*** - 0.493**
0.543* - 0.519*
0.351 - 0.424
n is the n u m b e r in each sample. * P < 0.05; **P< 0.01; ***P< 0.001.
332
I.M. TURNER
E T AL.
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Mycorrhizal Infect~n (%) Fig. 1. The relationship between (a) total dry mass and (b) root:shoot ratio and the extent of mycorrhizal infection for S. macroptera seedlings from Experiment 1. Closed symbols, control; open symbols, fertilized (NPK). Lines show linear regression fitted through all points. For total dry weight overall regression is y = 5.56 + 0.09x (r2= 0.369, P < 0.001 ); for control group alone y=4.46+0.13x (r2=0.618, P<0.001 ); for fertilized group alone y=7.42+0.06x (r2=0.124, P>0.05). For root:shoot ratio overall linear regression is y = 0 . 3 3 2 - 0 . 0 0 2 x (r2=0.208, P<0.01 ); for control alone y = 0 . 3 4 4 - 0 . 0 0 2 x (r2=0.305, P<0.05); for fertilized group alone y = 0 . 3 1 4 - 0 . 0 0 1 x (r2=0.05).
( ___0.9 ) g, respectively. These are not significantly different (Student's t-test; t = 1.07, P = 0.29). The fertilized seedlings had a mean extent of ECM infection of 53.7%, which was significantly higher than the mean infection of 37.5% in the control group ( t = 2.15, P < 0.05 ). The extent of infection was significantly correlated with
333
F E R T I L I Z E R E F F E C T S ON D I P T E R O C A R P S
total seedling dry mass at harvest (Table 1, Fig. 1 ). The correlation was only significant ( P < 0.05 ) for the unfertilized seedlings. There was also a clear negative correlation between root:shoot ratio and the extent of ECM infection, which again was only significant for the unfertilized seedlings when the analysis was broken down by treatment.
Experiment 2 No significant effects of fertilizer treatment on height or stem diameter growth of S. curtisii were recorded (Tables 2 and 3 ). This reflects at least in part, the high degree of variation in seedling growth within each plot. Seedling performance showed no relation to plot seedling density. TABLE 2 The effect of fertilizer addition on the growth of S. curtisii seedlings in l-m 2 plots in Pantai Acheh Forest Reserve, Penang, Malaysia (Experiment 2 ). Mean ± standard error Plot
Treatment ~
Number of seedlings
Height increment (cm)
Basal stem diameter increment ( mm )
1 2 3 4 5 6 7 8
C +N +P +N+P C +N +P +N+P
24 17 26 30 46 22 24 27
1.04_+0.19 0.53_+0.48 0.81 _+0.26 0.43_+0.17 0.93_+0.18 0.73_+0.35 0.71 _+0.22 1.30+_0.25
0.18_+0.04 0.13_+0.06 0.22+_0.03 0.12_+0.04 0.12_+0.03 0.16+0.07 0.08_+0.06 0.15_+0.04
~C is control; + N is N addition at 10 g m-2; + P is P addition at 5 g m -2.
TABLE 3 The effect of fertilizer addition on the growth of S. curtisii (Experiment 2): results of analyses of variance (ANOVA). F ratios are presented for the results given in Table 2 (the number of degrees of freedom is 1,7 in all cases). ANOVA after correction of data for covariate of initial height or initial basal stem diameter FACTORS N Height increment Basal stem diameter increment
< 0.001
P
N×P 0.516
0.515
n.s.
n.s.
n.s.
0.033 n.s.
< 0.001 n.s.
0.004 n.s.
n.s. indicates that the result is not significant ( P > 0.05 ).
334
I.M. TURNERETAL
(a) 50. 40,
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Fig. 2. Height growth of H. beccariana seedlings under canopy shade ( 100 seedlings per treatment) in Danum Valley Conservation Area, Sabah, Malaysia: (a) plot mean height growth; (b) plot mean relative height growth. Bars represent one standard error about the mean.
Experiment 3 The growth of the H. beccariana seedlings was alike under the two treatments in terms of mean height growth and mean relative height growth after 10 months (Fig. 2 ). DISCUSSION
Few firm conclusions can be drawn from a comparison of these three experiments, as they involved a variety of different designs, materials and growth
FERTILIZER EFFECTS ON DIPTEROCARPS
335
conditions. However, despite the preliminary nature of these investigations, some overall trends are apparent. Appreciable growth was observed to occur in all the experiments, indicating that the seedlings were not shaded severely enough to prevent growth. Young plants of two pioneer species, Melastoma malabathricum L. and Trema tornentosa (Roxb.) Hara, growing in the same soil showed a significant increase in growth following a fertilizer treatment similar to that received by the S. macroptera seedlings (Turner, 1991 ), making it unlikely that fertilizer immobilization was the cause of the observed lack of response in S. macroptera. The absence of a clear response to fertilizer application has been noted in some temperate trees (see Newton and Pigott, 1991 ) and in other tropical species. For example, Denslow et al. (1990) found that rooted cuttings of seven shrub species did not respond to fertilizer when planted out either in the understorey or in gaps in a Costa Rican rain forest. Plants from infertile sites generally exhibit limited responses to fertilizer addition, partly as ares ult of intrinsically low growth rates (Chapin et al., 1986 ). It may be the case that dipterocarps respond very little to increased availability other than at extreme deficiency levels but this clearly requires further investigation. Pot-grown dipterocarp seedlings have been shown to respond to rates of fertilizer application similar to those used in Experiment 1 (Madius Tangau, 1983; Sundralingam, 1983; Sundralingam et al., 1985). However, Sundralingam et al. (1985) and Madius Tangau (1983) used non-forest soils (sand culture and agricultural soil, respectively ) for their experiments. The nutrient status of these media may have been lower than that of the forest soils utilized in this investigation. However, no analyses of nutrient availability were performed in this study. In addition, seedlings grown in dipterocarp forest soil would presumably form mycorrhizas more readily than when grown in sterile sand or agricultural soils deficient in the appropriate fungal flora. The S. macroptera root systems in Experiment 1 had strongly developed ectomycorrhizas. The extent of ECM infection of these seedlings was higher when fertilized, an observation contrasting with other work on dipterocarps (Smits, 1987; Jiilich, 1988) and temperate ectomycorrhizal trees (Marx et al., 1977; Newton and Pigott, 1991 ). It is possible that in nutrient-poor soils fertilizers may thus facilitate ECM infection. For unfertilized S. macroptera seedlings, the extent of mycorrhizal infection was clearly related to growth, a result similar to that found by Becker ( 1983 ) for wild Shorea seedlings and Newton ( 1991 ) for Betula pendula Roth grown on P-deficient soil. Once fertilized, the extent of mycorrhizal infection was not significantly correlated with seedling growth. These results are supported by those of Lee and Lim (1989), who found that only Shorea seedlings from an interfile site (low P availability) showed a significant correlation between extent of ECM infection and foliar P concentration. Together, these results suggest that ECM infection may be important for seedling growth under conditions of low nu-
336
I.M. TURNER ET AL.
trient availability, but that this effect is reduced by fertilization. These preliminary results suggest that the addition of nutrients to promote higher growth rates in regenerating seedlings in dipterocarp forests is unlikley to be a viable silvicultural practice, although ensuring that there is adequate mycorrhizal infection in dipterocarp planting material may be beneficial. Further research on these aspects is clearly required before firmer management guidelines can be developed.
ACKNOWLEDGEMENTS
We are grateful to the Government of Malaysia for permission to conduct research in Malaysia and to the Natural Environment Research Council (UK) for financial support.
REFERENCES Ashton, P.S., 1989. Dipterocarp reproductive biology. In: H. Leith and M.J.A. Werger (Editors), Tropical Rain Forest Ecosystems. Elsevier, Amsterdam, pp. 219-240. Becker, P., 1983. Ectomycorrhizae on Shorea (Dipterocarpaceae) seedlings in a lowland Malaysian rainforest. Malays. For., 46: 146-170. Chapin, F.S., Vitousek, P.M. and van Cleve, K., 1986. The nature of nutrient limitation in plant communities. Am. Nat., 127: 48-58. Connell, J.H. and Lowman, M.D., 1989. Low-diversity tropical rain forests: some possible mechanisms for their existence. Am. Nat., 134: 88-119. Denslow, J.S., Schultz, J.C., Vitousek, P.M., and Strain, P.M., 1990. Growth responses of tropical shrubs to treefall gap environments. Ecology, 71: 165-179. Jtilich, W., 1988. Dipterocarpaceae and mycorrhizae. GFG Report No. 9, Indonesian-German Forestry Project, Mulawarman University, Samarinda, East Kalimantan, Indonesia, 103 pp. Lee, S.S., 1990. The mycorrhizal association of the Dipterocarpaceae in the tropical rain forests of Malaysia. Ambio, 19: 383-385. Lee, S.S. and Lim, K.L., 1989. Mycorrhizal infection and foliar phosphorus content of seedlings of three dipterocarp species grown in a selectively logged forest and a forest plantation. Plant Soil, 117: 237-241. Madius Tangau, 1983. Effect of soil moisture and fertilizer on the growth of Shorea bracteolata Dyer and Shorea parvifolia Dyer seedlings. B.Sc, Thesis, Faculty of Forestry, Universiti Pertanian Malaysia, Serdang, Malaysia. Marx, D.H., Hatch, A.B. and Mendecino, J.F., 1977. High soil fertility decreases sucrose content and susceptibility of loblolly pine roots to ectomycorrhizal infection by Pisolithus tinctorius. Can. J. Bot., 55: 1569-1574. Newton, A.C., 1991. Mineral nutrition and mycorrhizal infection of seedling oak and birch. III. Epidemioiogical aspects of ectomycorrhizal infection and the relation to seedling growth. New Phytol., 117: 53-60. Newton, A.C. and Pigott, C.D., 1991. Mineral nutrition and mycorrhizal infection of seedling oak and birch. II. The effect of fertilizers on growth, nutrient uptake and ectomycorrhizal infection. New Phytol., 117: 45-52.
FERTILIZER EFFECTS ON DIPTEROCARPS
3 37
Siew, K.Y., 1969. Present Land Use of Penang and Province Wellesley. Ministry of Agriculture and Co-operatives, Kuala Lumpur, Malaysia, 30 pp. Singh, K.F., 1966. Ectotrophic mycorrhiza in equatorial rain forest. Malay. For., 39:13-19. Stairs, W.T.M., 1985. Specificity ofdiptertocarp mycorrhiza. In: R. Molina (Editor), Proc. 6th North American Conf. on Mycorrhizae, 25-29 June 1984, Band, OR. Forest Research Laboratory, Oregon State University, Corvallis, OR, p. 364. Smits, W.T.M., 1987. Production of dipterocarp planting stocks in nurseries. In: A.J.G.H. Kostermans (Editor), Proc. 3rd Round-Table Conf. on Dipterocarps, 16-20 April 1985, Samarinda, Indonesia. UNESCO Regional Office for Science and Technology, Jakarta, Indonesia, pp. 153-157. Soong, N.K. and Lau, C.H., 1977. Physical and chemical properties of soil. In: E,Pushparajah and L.L. Amin (Editors), Soils under Hevea and their Management. Rubber Research Institute of Malaysia, Kuala Lumpur, pp. 25-26. Sundralingam, P., 1983. Response of potted seedlings of Dryobalanops aroma#ca and Dryohalanops oblongiJblia to commercial fertilizers. Malays. For., 46: 86-92. Sundralingam, P., Hotta, I. and Osumi, Y., 1985. Assessment of the nitrogen and phosphorus requirements of Shorea ovalis using sand culture. Malays. For., 48:314-323. Turner, I.M., 1989. An enumeration of one hectare of Pantai Aceh Forest Reserve, Penang. Gard. Bull. (Singapore), 42: 29-44. Turner, I.M., 1991. Effects of shade and fertilizer addition on the seedlings of two tropical woody pioneer species. Trop. Ecol., 32: 24-29. Whitmore, T.C., 1989. Southeast Asian tropical forests. In: H. Leith and M.J.A. Werger (Editors), Tropical Rain Forest Ecosystems, Elsevier, Amsterdam, pp. 195-218.
329
Elsevier Science Publishers B.V., Amsterdam
Short Communication
The effect of fertilizer application on dipterocarp seedling growth and mycorrhizal infection I.M. Turnera, N.D.
Brown b and A.C. Newton c
aDepartment of Botany, National University of Singapore, Lower Kent Ridge Road, Singapore 0511. Singapore bOxford Forestry Institute, University of Oxford, South Parks Road, Oxford OX1 3RB, UK Clnstitute of Terrestrial Ecology, Bush Estate, Penicuik, Ett26 OQB, UK (Accepted 13 August 1992)
ABSTRACT Turner, I.M., Brown, N.D. and Newton, A.C., 1993. The effect of fertilizer application on dipterocarp seedling growth and mycorrhizal infection. For.Ecol. Manage., 57: 329-337. In three independent experiments, application of fertilizers had no effect on the growth of dipterocarp seedlings. The experiments involved application of: ( 1 ) NPK at a rate of 10 g m -2 N, P205 and K20 to Shorea macroptera Dyer seedlings grown in pots of forest soil under nursery conditions in Penang, Malaysia; (2) N at a rate of 10 g m -2 and/or P at a rate of 5 g m -2 in a factorial design to 8month-old Shorea curtisii Dyer ex King seedlings growing wild in coastal hill dipterocarp forest in Penang, Malaysia; (3) NKP at a rate of 10 g m -2 three times over 10 months to Hopea beccariana Burck seedlings growing wild in lowland mixed dipterocarp forest in Sahah, Malaysia. In Experiment 1, fertilizer application significantly increased the extent of ectomycorrhizal (ECM) infection of the S. macroptera roots, and unfertilized seedlings showed a closer correlation between extent of ECM infection and growth than fertilized seedlings. These preliminary results suggest that dipterocarp seedlings may only be responsive to fertilizer addition when grown at very low nutrient availabilities, and that ECM infection may be of great importance to seedling growth under such conditions.
INTRODUCTION
The Dipterocarpaceae dominate the canopy of the lowland tropical rain forests of the Malay Peninsula, Sumatra, Borneo and the Philippines (Whitmore, 1989) and they currently supply over half of the World's hardwood (Ashton, 1989). Detailed information on the influence of environmental conditions on the growth and survival of juvenile dipterocarps is required, Correspondence to: I.M. Turner, Department of Botany, National University of Singapore, Lower Kent Ridge Road, Singapore 051 I. Fax, Singapore 779 5671.
© 1993 Elsevier Science Publishers B.V. All rights reserved 0378-1127/93/$06.00
330
I.M. TURNER ETAL.
particularly for the commercially most important groups such as the red meranti Shorea species. Little work has been carried out on the responses of dipterocarp seedlings to soil nutrient status. Dipterocarps have ectomycorrhizal (ECM) associations (Singh, 1966; Lee, 1990) which may be obligate for normal growth (Smits, 1985). ECM symbioses have been postulated to be the key to the dominance of the Dipterocarpaceae in Southeast Asia (Connell and Lowman, 1989). This paper presents the results of some preliminary experiments investigating the influence of fertilizer application on seedling growth in the nursery and in the forest. In one experiment the extent of ECM infection of the seedlings was assessed and related to fertilizer treatment. METHODS
Experiment 1 Forty seedlings of Shorea macroptera Dyer were grown from locally collected seed in polyethylene pots of sieved forest topsoil (about 1.5 1) under the shade of a large Eugenia grandis Wight tree at Muka Head Field Station, Penang, Malaysia. The seeds and soil were collected from under mature dipterocarps in the adjacent Pantai Acheh Forest Reserve. The soils of the Reserve are Typic Paleudults (Siew, 1969), a group which generally has moderate to low fertility in Peninsular Malaysia (Soong and Lau, 1977 ). At the start of the experiment half of the eight-month-old seedlings were randomly selected and given a fertilizer treatment of 10 g m-2 of combined N, P205 and KaO in the form of a proprietary N P K fertilizer (Wonder-Gro, The Agricultural Farming Co., Penang, Malaysia) in solution (equivalent to 100 mg of each of N, P and K per pot). Six months later, all the plants were harvested, dried in an 80°C oven for 2 days and weighed. Small samples (about ten 2-cm pieces of lateral root with their attached side-branches) of the root system of each S. macroptera seedling were taken during the harvesting and fixed in formyl acetic alcohol for subsequent analysis of ECM infection. Each sample was examined, immersed in water, under a × 6 - X 45 zoom objective. A series of randomly selected fields was assessed, until a total of more than 200 tips per sample had been counted. Infection was characterized by the presence of a complete fungal mantle on the root tip. The extent of infection was expressed as the percentage of root tips that were mycorrhizal, with the tips of branching mycorrhizas being counted separately.
Experiment 2 A population of Shorea curtisii Dyer ex King seedlings originating from natural regeneration, approximately eight months old at the start of the ex-
FERTILIZER EFFECTS ON DIPTEROCARPS
331
periment, was located in Pantai Acheh Forest Reserve, Penang, Malaysia, in a coastal hill dipterocarp forest (Turner, 1989). Eight 1 m × 1 m plots were laid out in the area, which was near a small canopy opening. Three fertilizer treatments were randomly assigned to the plots: NHaNO3 applied at a rate of 10 g m - 2 N, P205 applied at a rate of 5 g m - 2 p and a combined application of N and P at the above rates plus an unfertilized control. All treatments were replicated twice. All the seedlings, ranging from 17 to 46 per plot, were tagged, then heights and basal stem diameters were measured using vernier callipers. Fertilizer was applied dry, by the hand, to the surface of the soil in each plot. All the seedlings were remeasured after 5 months.
Experiment 3 One hundred wild Hopea beccariana Burck seedlings ranging from 130 m m to 1030 m m in height were tagged and measured in two 6-m 2 plots located under the closed canopy of primary lowland dipterocarp rain forest in the D a n u m Valley Conservation Area, Sabah, Malaysia. The two plots were aligned down a gentle slope (less than 3 ° ) and were separated by a distance of 1 m. The upslope plot had a canopy openness value (proportion of total sky unobscured by forest canopy) of 4.7% as determined from a vertical hemispherical photograph taken at the start of the experiment. The downslope plot had 2.5% canopy openness and was treated with 10 g m -2 of N P K fertilizer (Rustica 15:15:6:4, Ruhr-Stickstoff AG, Germany), broadcast evenly in dry pellet form at the start of the experiment. Further fertilizer applications were made at the same dosage 2.5 and 5 months later, at which time all the seedlings on both plots were remeasured for height. All seedlings were measured for a final time 10 months after the start of the experiment. RESULTS
Experiment I The mean (_+standard error) of the total dry mass of the fertilized and unfertilized groups of S. macroptera seedlings were 10.4 (_+0.8)g and 9.2 TABLE 1 T h e relationship between the extent o f m y c o r r h i z a l infection a n d growth o f pot-grown S. macroptera seedlings ( E x p e r i m e n t 1 ). S p e a r m a n ' s rank correlation coefficient
Total dry weight Root:shoot ratio
All seedlings n=401
Control group n=201
Fertilized group n=20 t
0.555*** - 0.493**
0.543* - 0.519*
0.351 - 0.424
n is the n u m b e r in each sample. * P < 0.05; **P< 0.01; ***P< 0.001.
332
I.M. TURNER
E T AL.
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80
100
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Mycorrhizal Infect~n (%) Fig. 1. The relationship between (a) total dry mass and (b) root:shoot ratio and the extent of mycorrhizal infection for S. macroptera seedlings from Experiment 1. Closed symbols, control; open symbols, fertilized (NPK). Lines show linear regression fitted through all points. For total dry weight overall regression is y = 5.56 + 0.09x (r2= 0.369, P < 0.001 ); for control group alone y=4.46+0.13x (r2=0.618, P<0.001 ); for fertilized group alone y=7.42+0.06x (r2=0.124, P>0.05). For root:shoot ratio overall linear regression is y = 0 . 3 3 2 - 0 . 0 0 2 x (r2=0.208, P<0.01 ); for control alone y = 0 . 3 4 4 - 0 . 0 0 2 x (r2=0.305, P<0.05); for fertilized group alone y = 0 . 3 1 4 - 0 . 0 0 1 x (r2=0.05).
( ___0.9 ) g, respectively. These are not significantly different (Student's t-test; t = 1.07, P = 0.29). The fertilized seedlings had a mean extent of ECM infection of 53.7%, which was significantly higher than the mean infection of 37.5% in the control group ( t = 2.15, P < 0.05 ). The extent of infection was significantly correlated with
333
F E R T I L I Z E R E F F E C T S ON D I P T E R O C A R P S
total seedling dry mass at harvest (Table 1, Fig. 1 ). The correlation was only significant ( P < 0.05 ) for the unfertilized seedlings. There was also a clear negative correlation between root:shoot ratio and the extent of ECM infection, which again was only significant for the unfertilized seedlings when the analysis was broken down by treatment.
Experiment 2 No significant effects of fertilizer treatment on height or stem diameter growth of S. curtisii were recorded (Tables 2 and 3 ). This reflects at least in part, the high degree of variation in seedling growth within each plot. Seedling performance showed no relation to plot seedling density. TABLE 2 The effect of fertilizer addition on the growth of S. curtisii seedlings in l-m 2 plots in Pantai Acheh Forest Reserve, Penang, Malaysia (Experiment 2 ). Mean ± standard error Plot
Treatment ~
Number of seedlings
Height increment (cm)
Basal stem diameter increment ( mm )
1 2 3 4 5 6 7 8
C +N +P +N+P C +N +P +N+P
24 17 26 30 46 22 24 27
1.04_+0.19 0.53_+0.48 0.81 _+0.26 0.43_+0.17 0.93_+0.18 0.73_+0.35 0.71 _+0.22 1.30+_0.25
0.18_+0.04 0.13_+0.06 0.22+_0.03 0.12_+0.04 0.12_+0.03 0.16+0.07 0.08_+0.06 0.15_+0.04
~C is control; + N is N addition at 10 g m-2; + P is P addition at 5 g m -2.
TABLE 3 The effect of fertilizer addition on the growth of S. curtisii (Experiment 2): results of analyses of variance (ANOVA). F ratios are presented for the results given in Table 2 (the number of degrees of freedom is 1,7 in all cases). ANOVA after correction of data for covariate of initial height or initial basal stem diameter FACTORS N Height increment Basal stem diameter increment
< 0.001
P
N×P 0.516
0.515
n.s.
n.s.
n.s.
0.033 n.s.
< 0.001 n.s.
0.004 n.s.
n.s. indicates that the result is not significant ( P > 0.05 ).
334
I.M. TURNERETAL
(a) 50. 40,
Unfertilized
E 30 0
g
2o
Fertilized
IE 10
'l =
I
I
I
I
0
I
I
1O0
I
I
I
I
I
I
200
Days
300
(b)
"" o . ~ 5 -
iiii
'~ O.lO0 I0}
Fertilized
o.o~
g O, "I"
I
0
I
f
I
100
i
t
Days
i
i
200
i
I
i
i
300
Fig. 2. Height growth of H. beccariana seedlings under canopy shade ( 100 seedlings per treatment) in Danum Valley Conservation Area, Sabah, Malaysia: (a) plot mean height growth; (b) plot mean relative height growth. Bars represent one standard error about the mean.
Experiment 3 The growth of the H. beccariana seedlings was alike under the two treatments in terms of mean height growth and mean relative height growth after 10 months (Fig. 2 ). DISCUSSION
Few firm conclusions can be drawn from a comparison of these three experiments, as they involved a variety of different designs, materials and growth
FERTILIZER EFFECTS ON DIPTEROCARPS
335
conditions. However, despite the preliminary nature of these investigations, some overall trends are apparent. Appreciable growth was observed to occur in all the experiments, indicating that the seedlings were not shaded severely enough to prevent growth. Young plants of two pioneer species, Melastoma malabathricum L. and Trema tornentosa (Roxb.) Hara, growing in the same soil showed a significant increase in growth following a fertilizer treatment similar to that received by the S. macroptera seedlings (Turner, 1991 ), making it unlikely that fertilizer immobilization was the cause of the observed lack of response in S. macroptera. The absence of a clear response to fertilizer application has been noted in some temperate trees (see Newton and Pigott, 1991 ) and in other tropical species. For example, Denslow et al. (1990) found that rooted cuttings of seven shrub species did not respond to fertilizer when planted out either in the understorey or in gaps in a Costa Rican rain forest. Plants from infertile sites generally exhibit limited responses to fertilizer addition, partly as ares ult of intrinsically low growth rates (Chapin et al., 1986 ). It may be the case that dipterocarps respond very little to increased availability other than at extreme deficiency levels but this clearly requires further investigation. Pot-grown dipterocarp seedlings have been shown to respond to rates of fertilizer application similar to those used in Experiment 1 (Madius Tangau, 1983; Sundralingam, 1983; Sundralingam et al., 1985). However, Sundralingam et al. (1985) and Madius Tangau (1983) used non-forest soils (sand culture and agricultural soil, respectively ) for their experiments. The nutrient status of these media may have been lower than that of the forest soils utilized in this investigation. However, no analyses of nutrient availability were performed in this study. In addition, seedlings grown in dipterocarp forest soil would presumably form mycorrhizas more readily than when grown in sterile sand or agricultural soils deficient in the appropriate fungal flora. The S. macroptera root systems in Experiment 1 had strongly developed ectomycorrhizas. The extent of ECM infection of these seedlings was higher when fertilized, an observation contrasting with other work on dipterocarps (Smits, 1987; Jiilich, 1988) and temperate ectomycorrhizal trees (Marx et al., 1977; Newton and Pigott, 1991 ). It is possible that in nutrient-poor soils fertilizers may thus facilitate ECM infection. For unfertilized S. macroptera seedlings, the extent of mycorrhizal infection was clearly related to growth, a result similar to that found by Becker ( 1983 ) for wild Shorea seedlings and Newton ( 1991 ) for Betula pendula Roth grown on P-deficient soil. Once fertilized, the extent of mycorrhizal infection was not significantly correlated with seedling growth. These results are supported by those of Lee and Lim (1989), who found that only Shorea seedlings from an interfile site (low P availability) showed a significant correlation between extent of ECM infection and foliar P concentration. Together, these results suggest that ECM infection may be important for seedling growth under conditions of low nu-
336
I.M. TURNER ET AL.
trient availability, but that this effect is reduced by fertilization. These preliminary results suggest that the addition of nutrients to promote higher growth rates in regenerating seedlings in dipterocarp forests is unlikley to be a viable silvicultural practice, although ensuring that there is adequate mycorrhizal infection in dipterocarp planting material may be beneficial. Further research on these aspects is clearly required before firmer management guidelines can be developed.
ACKNOWLEDGEMENTS
We are grateful to the Government of Malaysia for permission to conduct research in Malaysia and to the Natural Environment Research Council (UK) for financial support.
REFERENCES Ashton, P.S., 1989. Dipterocarp reproductive biology. In: H. Leith and M.J.A. Werger (Editors), Tropical Rain Forest Ecosystems. Elsevier, Amsterdam, pp. 219-240. Becker, P., 1983. Ectomycorrhizae on Shorea (Dipterocarpaceae) seedlings in a lowland Malaysian rainforest. Malays. For., 46: 146-170. Chapin, F.S., Vitousek, P.M. and van Cleve, K., 1986. The nature of nutrient limitation in plant communities. Am. Nat., 127: 48-58. Connell, J.H. and Lowman, M.D., 1989. Low-diversity tropical rain forests: some possible mechanisms for their existence. Am. Nat., 134: 88-119. Denslow, J.S., Schultz, J.C., Vitousek, P.M., and Strain, P.M., 1990. Growth responses of tropical shrubs to treefall gap environments. Ecology, 71: 165-179. Jtilich, W., 1988. Dipterocarpaceae and mycorrhizae. GFG Report No. 9, Indonesian-German Forestry Project, Mulawarman University, Samarinda, East Kalimantan, Indonesia, 103 pp. Lee, S.S., 1990. The mycorrhizal association of the Dipterocarpaceae in the tropical rain forests of Malaysia. Ambio, 19: 383-385. Lee, S.S. and Lim, K.L., 1989. Mycorrhizal infection and foliar phosphorus content of seedlings of three dipterocarp species grown in a selectively logged forest and a forest plantation. Plant Soil, 117: 237-241. Madius Tangau, 1983. Effect of soil moisture and fertilizer on the growth of Shorea bracteolata Dyer and Shorea parvifolia Dyer seedlings. B.Sc, Thesis, Faculty of Forestry, Universiti Pertanian Malaysia, Serdang, Malaysia. Marx, D.H., Hatch, A.B. and Mendecino, J.F., 1977. High soil fertility decreases sucrose content and susceptibility of loblolly pine roots to ectomycorrhizal infection by Pisolithus tinctorius. Can. J. Bot., 55: 1569-1574. Newton, A.C., 1991. Mineral nutrition and mycorrhizal infection of seedling oak and birch. III. Epidemioiogical aspects of ectomycorrhizal infection and the relation to seedling growth. New Phytol., 117: 53-60. Newton, A.C. and Pigott, C.D., 1991. Mineral nutrition and mycorrhizal infection of seedling oak and birch. II. The effect of fertilizers on growth, nutrient uptake and ectomycorrhizal infection. New Phytol., 117: 45-52.
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Siew, K.Y., 1969. Present Land Use of Penang and Province Wellesley. Ministry of Agriculture and Co-operatives, Kuala Lumpur, Malaysia, 30 pp. Singh, K.F., 1966. Ectotrophic mycorrhiza in equatorial rain forest. Malay. For., 39:13-19. Stairs, W.T.M., 1985. Specificity ofdiptertocarp mycorrhiza. In: R. Molina (Editor), Proc. 6th North American Conf. on Mycorrhizae, 25-29 June 1984, Band, OR. Forest Research Laboratory, Oregon State University, Corvallis, OR, p. 364. Smits, W.T.M., 1987. Production of dipterocarp planting stocks in nurseries. In: A.J.G.H. Kostermans (Editor), Proc. 3rd Round-Table Conf. on Dipterocarps, 16-20 April 1985, Samarinda, Indonesia. UNESCO Regional Office for Science and Technology, Jakarta, Indonesia, pp. 153-157. Soong, N.K. and Lau, C.H., 1977. Physical and chemical properties of soil. In: E,Pushparajah and L.L. Amin (Editors), Soils under Hevea and their Management. Rubber Research Institute of Malaysia, Kuala Lumpur, pp. 25-26. Sundralingam, P., 1983. Response of potted seedlings of Dryobalanops aroma#ca and Dryohalanops oblongiJblia to commercial fertilizers. Malays. For., 46: 86-92. Sundralingam, P., Hotta, I. and Osumi, Y., 1985. Assessment of the nitrogen and phosphorus requirements of Shorea ovalis using sand culture. Malays. For., 48:314-323. Turner, I.M., 1989. An enumeration of one hectare of Pantai Aceh Forest Reserve, Penang. Gard. Bull. (Singapore), 42: 29-44. Turner, I.M., 1991. Effects of shade and fertilizer addition on the seedlings of two tropical woody pioneer species. Trop. Ecol., 32: 24-29. Whitmore, T.C., 1989. Southeast Asian tropical forests. In: H. Leith and M.J.A. Werger (Editors), Tropical Rain Forest Ecosystems, Elsevier, Amsterdam, pp. 195-218.