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Plurality of tree species responses to drought perturbation in Bornean tropical rain forest

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Abstract

Drought perturbation driven by the El Niño Southern Oscillation (ENSO) is a principal stochastic variable determining the dynamics of lowland rain forest in S.E. Asia. Mortality, recruitment and stem growth rates at Danum in Sabah (Malaysian Borneo) were recorded in two 4-ha plots (trees ≥ 10 cm gbh) for two periods, 1986–1996 and 1996–2001. Mortality and growth were also recorded in a sample of subplots for small trees (10 to <50 cm gbh) in two sub-periods, 1996–1999 and 1999–2001. Dynamics variables were employed to build indices of drought response for each of the 34 most abundant plot-level species (22 at the subplot level), these being interval-weighted percentage changes between periods and sub-periods. A significant yet complex effect of the strong 1997/1998 drought at the forest community level was shown by randomization procedures followed by multiple hypothesis testing. Despite a general resistance of the forest to drought, large and significant differences in short-term responses were apparent for several species. Using a diagrammatic form of stability analysis, different species showed immediate or lagged effects, high or low degrees of resilience or even oscillatory dynamics. In the context of the local topographic gradient, species’ responses define the newly termed perturbation response niche. The largest responses, particularly for recruitment and growth, were among the small trees, many of which are members of understorey taxa. The results bring with them a novel approach to understanding community dynamics: the kaleidoscopic complexity of idiosyncratic responses to stochastic perturbations suggests that plurality, rather than neutrality, of responses may be essential to understanding these tropical forests. The basis to the various responses lies with the mechanisms of tree-soil water relations which are physiologically predictable: the timing and intensity of the next drought, however, is not. To date, environmental stochasticity has been insufficiently incorporated into models of tropical forest dynamics, a step that might considerably improve the reality of theories about these globally important ecosystems.

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Acknowledgements

We are grateful to the Danum Valley Management Committee and the Economic Planning Unit, Prime Minister’s Office, Malaysia, for permission to undertake this research; I. and S. Samat, J. Hanapi and N. Majid for recent field assistance; R. C. Ong (Sabah Forest Department) and G. Reynolds (Royal Society S.E. Asia Rain Forest Research Programme) for facilitating the work locally; E. J. F. Campbell, A. Hämmerli, D. N. Kennedy, G. H. Petol and M. J. Still of the 1986–1999 enumeration teams; C. E. Ridsdale (Rijksherbarium, Leiden) and L. Madani (SFD Herbarium, Sandakan) for tree identifications, especially the 2001 recruits; and R. P. D. Walsh for access to the Danum climate records. The research was funded by the Swiss National Science Foundation (grant nr 31–59088). This paper is a contribution to the Royal Society S. E. Asian Rain Forest Programme.

Author information

Correspondence to D. M. Newbery.

Appendices

Appendix 1

Climate

The low precipitation events at Danum 1985–2003

Eventa Start End Duration (d) DEFARH (mm)b
1 8/30/86 5/1/88 610 −905.1
2 11/7/88 12/7/88 31 −38.1
3 2/13/89 2/20/89 8 −7.5
4 3/29/89 5/13/89 44 48.9
5 6/1/89 6/6/89 6 n.a.c
6 10/23/90 3/23/93 883 −1,566.9
7 6/18/93 6/3/94 351 −357.3
8 6/15/94 6/23/94 9 −65.8
9 9/15/94 9/23/94 5 −17.8
10 10/25/94 11/1/94 6 −28.5
11 4/2/95 5/27/95 56 −8.6
12 6/29/95 8/13/95 44 −91.8
13 1/18/97 4/15/99 818 −1,846.0
14 3/18/02 6/26/02 101 −25.4
15 7/10/02 9/2/02 54 21.7
16 11/1/02 11/25/02 23 −73.9
17 12/4/02 3/26/03 112 −126.4
18 6/27/03 6/29/03 3 9.8
19 9/3/03 9/26/03 24 17.0
  1. aWhen ARA 365 < 0
  2. b(Total DRA) when ARA 365 < 0 and R 30  < 232 mm
  3. cARA365 < 0 but R30 > 232 mm across all 6 days

Appendix 2

Trees

Appendix 2(a) Sample sizes at the start of the periods P1 and P2 (n 86, n 96) and corresponding numbers of valid trees (nv P1, nv P2) for the calculation of annualized mortality (m a; % year−1) and recruitment (r a; % year−1) rates, and relative (rgr; mm m−1 year−1) growth rates, in periods P1 and P2 for the 34 most abundant species (and their families) at Danum

Species Family* m a and r a rgr
n 86 n 96 nv P1 nv P2
Alangium javanicum Alan 101 91 69 60
Antidesma neurocarpum Euph 119 100 77 70
Aporosa falcifera Euph 261 238 157 143
Ardisia sanguinolenta Myrs 568 591 430 444
Baccaurea tetrandra Euph 250 233 189 168
Barringtonia lanceolata Lecy 141 147 129 120
Chisocheton sarawakanus Meli 155 150 116 105
Cleistanthus contractus Euph 289 273 223 212
Dacryodes rostrata Burs 153 145 130 118
Dimorphocalyx muricatus Euph 840 801 667 645
Dysoxylum cyrtobotryum Meli 170 155 129 122
Fordia splendidissima Legu 520 543 394 414
Gonystylus keithii Thym 121 126 104 101
Knema latericia Myri 141 166 128 140
Lithocarpus nieuwenhuisii Faga 125 115 94 70
Litsea caulocarpa Laur 322 319 197 215
Litsea ochracea Laur 163 147 115 95
Lophopetalum beccarianum Cela 234 267 200 221
Madhuca korthalsii Sapo 508 532 433 429
Mallotus penangensis Euph 204 233 172 196
Mallotus wrayi Euph 2,268 2,207 1,781 1,723
Maschalocorymbus corymbosus Rubi 403 335 245 243
Parashorea malaanonan Dipt 149 133 111 93
Pentace laxiflora Tili 240 214 163 145
Polyalthia cauliflora Anno 324 302 271 258
Polyalthia rumphii Anno 141 138 119 119
Polyalthia sumatrana Anno 222 221 192 186
Polyalthia xanthopetala Anno 241 223 172 156
Reinwardtiodendron humile Meli 262 221 166 140
Shorea fallax Dipt 371 395 264 298
Shorea johorensis Dipt 197 157 82 72
Shorea parvifolia Dipt 206 170 124 104
Syzygium elopurae Myrt 134 120 100 97
Syzygium tawaense Myrt 124 120 85 74
Totals   10,667 10,328 8,028 7,796
  1. * Family abbreviations; Alan, Alangaceae; Anno, Annonaceae; Burs, Burseraceae; Cela, Celastraceae; Dipt, Dipterocarpaceae; Euph, Euphorbaceae; Faga, Fagaceae; Laur, Lauraceae; Lecy, Lecythidaceae; Legu, Leguminosae; Meli, Meliaceae; Myrs, Myrsinaceae; Myrt, Myrtaceae; Rubi, Rubiaceae; Sapo, Sapotaceae; Thym, Thymelaceae; Tili, Tiliaceae

Appendix 2(b) Sample sizes at the starts of period P1 (n 86) and sub-periods P2a and P2b (n 96, n 99) and corresponding numbers of valid trees (nv P1, nv P2a , nv P2b ) for the calculation of annualized mortality rates (m a; % year−1), and relative growth rates (rgr, mm m−1 year−1), for the 22 most abundant species within subplots at Danum

Species m a rgr
n 86 n 96 n 99 nv P1 nv P2a nv P2b
Aporosa falcifera 74 65 62 57 54 57
Ardisia sanguinolenta 166 138 130 125 114 109
Baccaurea tetrandra 76 66 62 57 52 55
Cleistanthus contractus 118 103 97 85 75 86
Dacryodes rostrata 58 54 48 51 45 40
Dimorphocalyx muricatus 276 250 236 227 209 213
Dysoxylum cyrtobotryum 53 41 36 39 32 32
Fordia splendidissima 157 134 122 119 105 101
Litsea caulocarpa 105 72 56 66 52 46
Litsea ochracea 60 49 45 47 42 35
Lophopetalum beccarianum 71 66 63 64 60 56
Madhuca korthalsii 112 103 98 97 89 86
Mallotus penangensis 57 48 45 48 44 44
Mallotus wrayi 713 612 573 569 517 493
Maschalocorymbus corymbosus 120 80 71 65 58 52
Pentace laxiflora 58 36 31 34 27 26
Polyalthia cauliflora 123 108 104 104 97 94
Polyalthia rumphii 53 48 47 46 45 41
Polyalthia sumatrana 50 43 36 45 35 31
Polyalthia xanthopetala 59 42 32 41 30 26
Reinwardtiodendron humile 76 55 48 49 42 40
Shorea fallax 85 64 55 62 51 43
Totals 2,720 2,277 2,097 2,097 1,875 1,806

Appendix 3

Tests

Appendix 3(a) Means (±SE) of 34-spp pair-wise correlations (n = 528) for each of four dynamics variables and % variance accounted for by first three axes of corresponding principal components analyses

  Coefficient r 1* 2 3
m a −0.014358 ± 0.000732 3.48 3.41 3.35
r a −0.014434 ± 0.000738 3.49 3.43 3.41
rgr −0.014838 ± 0.000778 3.49 3.39 3.35
cmp −0.014510 ± 0.000777 3.55 3.42 3.37
  1. * % Var. = 100/34 = 2.94 had all axes been equal

Appendix 3(b) Species which had significant differences in their dynamics variables from random expectation adjusted for multiple hypothesis testing: 34 species in plots

Variable Species codes# Holm (Sidak) adjusted P Family-wise P
m a bl 0.001508 0.0068
r a af, dr, px,se, st 0.001605 0.0068
kl 0.001767 0.0116
bt,cc 0.001804 0.0220
rgr dm 0.001508 0.0068
cmp dm 0.001508 0.0068
  1. # species codes are those of Table 2 in the main text
  2. The Benjamini-Hochberg step-up FDR procedure gave the same results as the Holm step-down one for m a and cmp; but for r a three further species were significant: pc, pl and sp (adjusted P = 0.0132, 0.0147 and 0.0162 resp.), and for rgr there was one further case: mw (adjusted P = 0.0029). Note that mw was ranked 4th highest yet was significant (unlike pr and cs) due to its very much larger population size (maximum in Appendix 2)

Appendix 3(c) Species which had significant differences in their rgr from random expectation adjusted for multiple hypothesis testing: 22 species in subplots

Period Species codes# Holm (Sidak) P Family-wise P
P1-P2a rh 0.002329 0.0044
P2a-P2b rh 0.002329 0.0044
dm 0.002440 0.0042
P1-P2b dm 0.002329 0.0044
mw 0.002440 0.0084
sf 0.002500 0.0400
  1. # Species codes are those of Table 2 in main text
  2. The FDR procedure resulted in the same results, i.e. no additionally significant species

Appendix 3(d) Bonferroni minimum P-critical values from the step-down FDR procedure which are used in the Bernoulli formula

  1. 1.

    P1 − P2: m a, 0.0002; r a, 0.0152; rgr, 0.0024; cmp, 0.0024

  2. 2.

    Rgr: P1 − P2a, 0.0002; P2a − P2b, 0.0002; P1 − P2b, 0.0020

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Newbery, D.M., Lingenfelder, M. Plurality of tree species responses to drought perturbation in Bornean tropical rain forest. Plant Ecol 201, 147 (2009). https://doi.org/10.1007/s11258-008-9533-8

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Keywords

  • Dynamics
  • Ecosystem
  • El Niño
  • Resilience
  • Stem growth
  • Tree mortality