Identification of functional groups in an old-growth tropical montane rain forest on Hainan Island, China

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Forest Ecology and Management 255 (2008) 1820–1830 www.elsevier.com/locate/foreco

Identification of functional groups in an old-growth tropical montane rain forest on Hainan Island, China Fuying Deng a, Runguo Zang a,*, Boping Chen b a

Key Laboratory of Forest Ecology and Environment, The State Forestry Administration, Institute of Forest Ecology, Environment and Protection, Chinese Academy of Forestry, Beijing 100091, China b School of Foreign Language, Central University of Nationalities, Beijing 100081, China Received 8 October 2006; received in revised form 4 December 2007; accepted 6 December 2007

Abstract Tropical forests have important roles in conserving global biodiversity and maintaining the functions of the earth’s ecosystems. Functional classification of the diverse tropical plant species will lay a good foundation for analysis of tropical forest ecosystems. In this study in an old-growth tropical montane rain forest on Hainan Island, China, we categorized the forest plants (including 252 tree species) into a few functional groups and analyzed their distributions in relation to different environmental factors. Thirteen functional groups were identified using principal components analysis (PCA) and the two-way indicator species analysis (TWINSPAN) program according to seven functional traits: growth form, potential height, buttress size, leaf phenology, seed mass, dispersal agent and wood density. With the exception of shrubs, functional groups (trees, palms, lianas, herbs and epiphytes) were more abundant in the ravine stands than in the mountain slope stands. Buttress size, potential height and seed mass were the key traits for functional group identification, and there were significant positive correlations among them. The ravine stands were composed mainly of functional groups with larger buttress and greater potential height, while the mountain slope stands were composed mainly of functional groups with greater seed mass. The functional groups in the canopy layer (usually composed of species with large buttress, great potential height or large seed mass) could well reflect differences of environmental factors. # 2007 Elsevier B.V. All rights reserved. Keywords: Functional group; Old-growth tropical montane rain forest; Mountain slope forest stands; Ravine forest stands; Functional traits; Environmental factors

1. Introduction Functional groups are defined as groups of species either exhibiting similar responses to an environment or having similar effects on major ecosystem processes (Kelly and Bowler, 2002; Lavorel and Garnier, 2002). Plant functional groups are considered to be a powerful link bridging the gap between plant physiology and ecosystem processes (Diaz and Cabido, 1997), and provide a promising framework for predicting ecosystem response to human-induced global changes (Craine et al., 2001; Lavorel and Garnier, 2002). However, establishing the rules for classifying species into functional groups is one of the most difficult practical problems to be faced in current studies, and there are many obstacles to develop effective functional classification schemes (Naeem and Wright, 2003).

* Corresponding author. Tel.: +86 10 6288 9546; fax: +86 10 6288 4972. E-mail address: [email protected] (R. Zang). 0378-1127/$ – see front matter # 2007 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2007.12.004

Since any species performs many ecological functions simultaneously, the identification of functional groups will often depend largely on the objectives and context of the classification (Noble and Gitay, 1996; Solbrig, 1994). At present, functional group classification is decided mainly on the basis of plant functional traits (Cornelissen et al., 2003), such as growth form, nitrogen fixation, wood density, seed size, leaf character, etc. (Hooper and Vitousek, 1997; Poorter et al., 2006; Reich et al., 2004; Wright et al., 2006). The grouping has been done mostly on the basis of the indirect relations between biological traits and ecosystem functioning. Compared with the traditional study of community ecology, this method can better explain the ecological process from the plant individual level to the ecosystem level, and can provide a new method for land ecology (McGill et al., 2006; Westoby and Wright, 2006). The tropical forest in China is located at the northern edge of the Indo-Malayan rain forest, whose species composition and community structure are relatively distinct from typical Asian tropical forests (Hu and Li, 1992; Zhang, 1995). The species distribution, community structure, dynamics and diversity of

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the tropical rain forests have been studied (Jiang and Lu, 1991; Lu et al., 1986; Zang et al., 2001; Zeng et al., 1997; Zhang, 1995). However, those studies were based mostly on the taxonomic system rather than on plant functional traits. Information about the general plant traits and functional characteristics of the tropical forest on Hainan Island is very limited. A functional classification for the plant species in this forest has not been reported. In this study, we identified the main functional groups in the forest, and analyzed their relations with different environmental factors. Our objectives were (1) to develop a system of identifying functional groups in the species-rich tropical montane rain forest on Hainan Island in China, which might be extended to other species-rich plant communities; (2) to understand the change of functional groups along major environmental gradients; and (3) to establish basic foundations for further studying the ecosystem functioning of tropical forests in China and their dynamics with anthropogenic disturbance (such as logging and plantation development) and global climate change. First, we classified the plant species into six growth forms (trees, shrubs, palms, lianas, herbs and epiphytes) and analyzed their relations with environmental factors. Then, focusing on the functional classification of tree species and their relations with the environment, principal components analysis was used to analyze the relations between the tree functional traits, and the program two-way indicator species analysis was used to classify trees into eight functional groups according to their six key functional traits. Finally, nonmetric multidimensional scaling (NMS) was applied to identify the relations between functional group distribution and environmental factors. 1.1. Study site The study site was on Hainan Island in an old-growth tropical montane rain forest in the Bawangling Nature Reserve (BNR) (188500 –198050 N, 1098050 –1098250 E), which is the most

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typical and primary tropical montane rain forest in China. Most of the forests in this reserve have not experienced human disturbance except for occasional hunting and gathering by the indigenous people. The population of these people has always been very small, so their influence on the forest has been very limited. Most of the forests in the reserve are now in a natural old-growth state, and are among the best-protected and most typical tropical montane rain forests (Zhang, 1995). The elevation ranges from 900 m to 1400 m. The soil supporting the forests is montane lateric soil. The climate is tropical monsoon, with an annual average air temperature of 23.6 8C (maximum, 36 8C; minimum, 17 8C), and the annual precipitation ranges from 1500 mm to 2000 mm, with an average of 1750 mm (Jiang et al., 2002). The old-growth tropical montane rain forest in the study area can be divided roughly into two major types of forest stands according to their site conditions and species composition, i.e. the mountain slope forest stands and the ravine forest stands. 1.2. Field data collection In total, 6 ha of forest was surveyed in six plots, including 4 ha of mountain slope forest stands (M1, M2, M3 and M4) and 2 ha of ravine forest stands (R1 and R2). Each plot consisted of 100 grid quadrants of 10 m  10 m. In each quadrant, the species of each plant was identified in terms of different growth forms: i.e. tree, shrub, liana, herb, epiphyte or palm. The diameter at breast height (DBH) and the height were measured for all trees >1.5 m in height. The number of each species was recorded for shrubs, lianas, herbs, epiphytes and palms. The conditions of each plot were recorded, including slope, aspect and elevation. A composite soil sample (0–20 cm depth) was collected from five random points and analyzed for pH, percentage of organic matter, available nitrogen, total nitrogen, available phosphorus, total phosphorus, and available potassium (Table 1). Plot M1 contained mainly Castanopsis hystrix,

Table 1 Summary of the six plots surveyed in the old-growth tropical montane rain forest Factors (abbreviation and unit)

M1

Topography Elevation (m) Landforma Aspectb Slope (8) Stone (%) Wet class c

1000 3 1 10 5 2

Soil pH Available phosphorus (P, mg kg1) Total phosphorus (TP, mg kg1) Available nitrogen (N, mg kg1) Total nitrogen (TN, mg kg1) Organic matter (SOM, %) Available potassium (K, mg kg1)

4.82 9.36 180.25 183.26 1410.5 3.61 87.04

a b c

M2 900 2 2 18 5 3 4.91 9.37 148.80 170.47 1420.4 3.47 105.85

M3 1300 3 3 15 5 1 4.51 17.33 171.28 244.97 2129.8 5.08 72.41

Landform: 1, valley bottom; 2, draw or slope of draw; 3, ridge. Aspect: 1, south west; 2, south or west; 3, north west or south east; 4, north; 5, north east. The wet class (1–5): increases with the distance from mountain to ravine.

M4 980 2 4 55 8 4 4.94 10.40 184.72 201.26 1512.4 3.46 107.66

R1 960 1 2 30 70 5 5.46 15.07 365.76 222.72 1815.8 3.66 165.30

R2 870 1 2 40 80 6 6.08 11.26 376.15 256.53 1830.7 3.37 152.95

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Table 2 Functional traits for the identification of functional groups among 252 plant species Type

Traits (abbreviation)

Life form Morphology (tree)

Regeneration (tree) a b

Level 6

1: 2: 3: 4:

Potential height (PHeight, m) Buttress size class (L/Da) Wood densityb (WDensity, g/cm3) Defoliate or green (DGreen)

5: Seed mass (SMass, g) 6: Dispersal agent (DAgent)

Categories 1: Tree; 3: shrub; 4: liana; 5: grass; 6: epiphyte; 7: palm

2

Original continuous data 1: L/D < 1; 2: L/D < 2; 3: L/D < 3; 4: L/D  4; 5: L/D  5 Original continuous data 1: Defoliate (yes = 1, no = 0); 2: green (yes = 1, no = 0)

4 1

Original continuous data 1: Wind (yes = 1, no = 0); 2: auto (yes = 1, no = 0); 3: animal (yes = 1, no = 0)

5

Buttress size (L/D): ratio of the distance of the biggest buttress from the tree center to the diameter at basal height. Wood density: at 12% moisture (or air dry timber).

Lithocarpus fenzelianus and Mallotus hookerianus. The dominant species in plots M2 and M4 were not obvious. M2 contained C. hystrix, Lindera kwangtungensis and Symphyllia silhetiana. M4 contained L. kwangtungensis, Elaeocarpus apiculatus and Wrightia laevls. Plot M3 contained mainly Dacrydium pierrie and Syzygium araiocladum. Plots R1 and R2 contained mainly E. apiculatus and Homalium hainanense. 1.3. Selection of plant functional traits First, the species of the old-growth tropical montane rain forest were classified into six different growth forms: trees, shrubs, palms, lianas, herbs and epiphytes. Given the lack of functional traits for palms, shrubs, herbs, lianas and epiphytes, and their low abundance, this study was focused mainly on tree species for detailed classification of functional groups on the basis of morphology, regeneration traits and wood density. The morphological traits include potential height, buttress size and leaf phenology (deciduous versus evergreen), and regeneration traits include seed mass and dispersal agent. These plant functional traits are used widely, are easy to measure, and there is a great deal of data available. The potential height of a species (Hmax) was obtained from the average height of the 20 tallest specimens in each plot, and such materials as Flora Hainanica (Chun, 1964, 1965; Guangdong Institute of Botany, 1974, 1977) were used as references. Wood density (at 12% moisture content or air dry timber) was taken mainly from Hainan Timber: Discrimination, Character and Using (Joint Working Group of Hainan Timber Research, 1966) and Wood Density Data of World Agroforestry Centre (http:// www.worldagroforestrycentre.org/sea/Products/AFDbases/ WD/Index.htm). Data for seed mass were from Seeds of Woody Plants in China (State Forestry Administration, 2001) and the Kew Gardens Seed Information Database (http://www.rbgkew. org.uk/data/sid/). Seed dispersal agents were determined from flower colors, fruit types and structure, which included dispersal by wind, auto and animal. Species were classified as evergreen or deciduous on the basis of the level of deciduousness in the dry season. Some species may be partially deciduous, and the same species may have different levels of deciduousness in different years or in different environments (Condit et al., 2000). We defined deciduous species to include complete deciduousness and loss of >50% of leaves.

1.4. Data analysis The distributions of growth forms in the forest were analyzed by the Kruskal–Wallis test. The relations between growth forms and environmental factors were analyzed by Pearson’s correlation coefficient. In order to classify tree species into different functional groups and to analyze their relations with the environment, a relational database was constructed, containing the following information: (1) taxaspecific traits (252 species, 6 traits) (Table 2); (2) plot compositions (6 plots, 252 species); and (3) environmental characters of plots (6 plots, 13 environmental factors). To remove the influence of dimension, the numerical data in the matrices, including potential height, wood density, seed mass, elevation and soil nutrient (buttress size was recorded as ordinal data, ranging from 1 to 5, so we did not transform them) were transformed with log10. If the variable was not numerical, we assigned present/absent (0/1) scores: defoliate, yes/no = 1/0; evergreen, yes/no = 1/0; auto dispersal, yes/no = 1/0; wind dispersal, yes/no = 1/0; animal dispersal, yes/no = 1/0. The relations between the taxa-specific tree functional traits were examined by PCA for 252 tree species. The PCA was conducted on a correlation matrix (Pearson’s correlation coefficient) of the classified data (Table 2), which allowed us to identify the key tree functional traits that led to differences between species. In the ordination figure, the length of the arrowed line was proportional to the contribution of the factor to classification, the angle between the line and the ordination axis showed the closeness of the correlation, and the direction of the arrow showed whether the correlation was positive or negative. With the identified key functional traits, TWINSPAN analysis was used to identify functional groups at the third splitting level, as further splitting will lead to a large number of groups, each consisting of only a few species. NMS is a complex iterative technique for the analysis of non-linear data. This study used NMS to rank the functional groups in different plots on the basis of their relative basal area (i.e. the basal area of the given functional group compared with the total basal area in the stand) so as to represent the relations between different functional groups and their response to different environments. Correlation analysis (Pearson’s correlation coefficient) was used to understand the relations between the relative basal area of each functional group and the

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Fig. 1. Relative abundance of growth forms in different parts of a tropical montane old-growth forest. M1–M4, the mountain slope forest stands; R1 and R2, the ravine forest stands. Growth forms: E, epiphyte; G, grass; L, liana; P, palm; S, shrub; T, tree.

environmental factors, in order to identify the functional groups that could reflect changes of the environment. Differences of soil nutrients are closely related to different species compositions and environments. The mountain slope stands (M1, M2 and M4) and the ravine stands (R1 and R2) dominated by broadleaf trees differed in soil nutrients, as shown by a comparison using the Mann–Whitney U-test. The CANOCO program (ter Braak and Smilauer, 2003) was used to perform PCA. The PC-ORD program (McCune and Mefford, 1999) was used to perform TWINSPAN and NMS. Other statistical analyses were done with the SPSS package (SPSS, 2004). 2. Results 2.1. The abundance of functional groups based on different growth forms and their relations with environmental factors The abundance of functional groups based on different growth forms had significantly different distributions (Fig. 1; trees: x2 = 61.85, P < 0.0001; shrubs: x2 = 340.45,

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P < 0.0001; palms: x2 = 204.92, P < 0.0001; lianas: x2 = 217.31, P < 0.0001; herbs: x2 = 297.78, P < 0.0001; epiphytes: x2 = 51.12, P < 0.0001). Trees and shrubs were the most abundant plant types in the tropical montane forest, then lianas and herbs, and then palms and epiphytes. Among them, trees, palms, herbs, lianas and epiphytes were more abundant, and shrubs were less abundant, in ravine forest stands than in mountain slope forest stands. Correlation analysis between different functional groups based on abundance of growth form and environmental factors showed (Table 3) that trees were positively correlated with available P and total N; herbs were positively correlated with stone content and soil N; epiphytes and palms were positively correlated with the wet class and pH; and epiphytes were positively correlated with stone content, while shrubs were negatively correlated with the wet class, pH and stone content; and lianas were not correlated significantly with any environmental factor. 2.2. Functional groups of tree species identified by PCA and TWINSPAN According to PCA analysis based on morphology (buttress size and potential height), regeneration traits (seed mass and seed dispersal agent) and wood density of tree species, the first two axes in the figure estimated 85.1% of the variation of species composition (Fig. 2). Axis 1, representing the gradient change of seed mass and wood density, explained only 25.1% of the total variability. From left to right, with decreasing wood density and seed mass, the functional groups of FG2, FG4, FG6 and FG8 changed to FG1, FG3, FG5 and FG7. Axis 2 represents a gradient change in buttress size and potential height, which explained 59.2% of the total variation. From down to up, the buttress size and potential height increased significantly, FG8 and FG7 changed to FG6 and FG5, then to FG4 and FG3, and last FG2 and FG1. Further analysis showed that the correlations among buttress size, potential height and seed mass were significant

Table 3 Correlations between environmental factors and relative abundance of growth forms Correlations (abbreviation and unit)

Tree

Shrub

Palm

Liana

Grass

Epiphyte

Elevation (m) Landforma Aspectb Slope (8) Stone (%) Wet classc Elevation (m) Available phosphorus (P, mg kg1) Total phosphorus (TP, mg kg1) Available nitrogen (N, mg kg1) Total nitrogen (TN, mg kg1) Organic matter (SOM, %) Available potassium (K, mg kg1)

0.09 0.24 0.33 0.03 0.27 0.09 0.09 0.89* 0.14 0.77 0.94** 0.26 0.03

0.89* 0.96** 0.03 0.60 0.82* 0.89* 0.89* 0.31 0.60 0.43 0.37 0.49 0.83*

1.00** 0.84 0.21 0.43 0.64 0.83* 0.83* 0.14 0.43 0.09 0.03 0.71 0.71

0.26 0.48 0.03 0.66 0.27 0.43 0.43 0.20 0.20 0.43 0.43 0.09 0.66

0.43 0.72 0.27 0.49 0.82* 0.66 0.66 0.77 0.71 0.89* 0.83 0.14 0.60

0.54 0.84* 0.33 0.71 0.94** 0.83* 0.83* 0.60 0.83* 0.77 0.66 0.37 0.77

Bold values are significance at P < 0.05; *P < 0.05, **P < 0.01. a Landform: 1, valley bottom; 2, draw or slope of draw; 3, ridge. b Aspect: 1, south west; 2, south or west; 3, north west or south east; 4, north; 5, north east. c The wet class: determined from the distance to ravine, decreases with the distance.

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Fig. 2. Functional traits of species in the first two axes of the PCA. Buttress size was the ratio of the distance of the biggest buttress from the center of the tree to the DBH; the potential height (PHeight) was transformed with log10. FG1–FG8, functional groups. Functional traits: PHeight, potential height; buttress, buttress size; WDensity, wood density; SMass, seed mass; animal, animal dispersal; wind, wind dispersal; auto, auto dispersal; defoliate and green.

(P < 0.05), buttress size and potential height were correlated only weakly with other functional traits (P > 0.05), while seed mass was correlated significantly with wood density and seed dispersal agent (P < 0.05), and wood density was correlated significantly with leaf trait (deciduous or evergreen; P < 0.05). Eight functional groups were identified by TWINSPAN at the third splitting level (Table 4), and the species were classified first on the basis of buttress size and potential height, then reclassified on the basis of seed mass. FG1 consisted of emergent trees with the biggest buttress and maximum potential height, but different seed mass. They were all dominant components of the ravine stands, including mainly species such as Elaeocarpus subglobosus,

E. apiculatus, H. hainanense. FG2, FG3 and FG 4 were distributed mainly in the upper canopy layer of the forest. Their buttress size and potential height were next to that of FG1. FG2 was composed of the species with greatest seed mass, such as C. hystrix, Castanopsis tonkinensis, L. fenzelianus, D. pierrie located mainly in the mountain slope stands with greater elevation and drier climate. FG3 contained the species with the least seed mass, such as Ficus glaberrima and Ficus variegata, and were distributed mainly in the ravine stands with higher humidity. FG4 was composed of the species with moderate seed mass, such as L. kwangtungensis and W. laevis, and were distributed mainly in the mountain slope stands with higher humidity. FG5, FG6, FG7 and FG8 were composed of the species with no or small buttress and moderate seed mass. The seed mass of FG7 was less than that of FG8, both of which were distributed in the lower canopy. The seed mass of FG5 was less than that of FG6, both of which were distributed in the lowest layer of the forest. 2.3. The main environmental factors affecting the distribution of functional groups According to NMS based on relative basal area, the relations between environmental factors and functional group distribution are shown in Fig. 3. Axis 1 explained 50.3% of the total change. From left to right, decrease in elevation, stone content, pH, total P, available K and available N, for the ravine and mountain slope stands, respectively. Axis 2 explained 28.9% of the total change. From down to up, decrease in elevation and organic matter, mountain slope stands M3 changed to other forest stands. Further analysis showed that the mountain slope stands had less soil nutrients than the ravine stands, and a

Table 4 Characteristics and respective species of different functional groups (FGs) produced by TWINSPAN and PCA for the set of 252 species in the old-growth tropical montane forest Functional group (abbreviation)

MButtressa (rangeb, class)

High canopy and large buttress (FG1)

5 (2–5)

Canopy and big buttress Heavy smass (FG2) Light smass (FG3) Middle smass (FG4)

MSMass (range, g)

Respective species

26 (14–31)

130 (0.13–2000)

Homalium hainanense, Elaeocarpus apiculatus

4 (4–4) 3 (2–5) 3 (1–4)

26 (16–29) 21 (11–26) 21 (14–28)

1000 (7482–7500) 0.53 (0.39–0.96) 200 (10–2200)

Dacrydium pierrie, Cyclobalanopsis blakei Ficus glaberrima, Ficus variegata Lindera kwangtungensis, Wrightia laevis

Understory and small buttress Light smass (FG5) Heavy smass (FG6)

2 (2–2) 2 (1–2)

17 (14–19) 17 (14–19)

83 (0.13–320) 130 (30–1900)

Alangium salviifolium, Oreocnide rubescens Litseabaviensis, Symphyllia silbhtiana

Lower storey and no buttress Light smass (FG7) Heavy smass (FG8)

1 (1–1) 1 (1–1)

16 (11–24) 16 (11–23)

35 (0.1–450) 140 (0.13–6600)

Evodia meliadefolia, Sapium sebiferrum Symplocos caudate, Acronychia pedunculata

Shrub (FG9) Palm (FG10) Liana (FG11) Herbage (FG12) Epiphyte (FG13)

1 1 1 1 1

nmc nm nm nm nm

Saprosma ternatum, Psychotria rubra Rhapis excelsa, Livistona saribus Strixis suavolens, Ficus pumila Peristrophe montan, Lophatherum gracile Scindapsus maclurel, Asplenium antiquum

a b c

(1–1) (1–1) (1–1) (1–1) (1–1)

MPHeight (range, m)

<10 <30 <30 <10 <30

MButtress (MHeight, MDensity): mean buttress size (potential height, wood density). Range: min–max. nm: the lacking value.

F. Deng et al. / Forest Ecology and Management 255 (2008) 1820–1830

Fig. 3. NMS ordination for six plots in a tropical montane old-growth forest and environmental factors. Species relative area in 100 m  100 m quadrants were used to compute the ordinations in four dimensions. Both species scores and quadrant scores for the first two ordination axes are plotted. Mean concentrations of environmental factors in 100 m  100 m quadrants were fit to the ordination to test the relations between species composition and environmental factors. The orientation of arrows indicates the direction in ordination space in which the environmental factors change most rapidly and in which they have maximum correlation with the ordination configuration, whereas the length of the arrows indicates the rate of change (M1–M4, the mountain slope forest stands; R1 and R2, ravine forest stands). Environmental factors: elevation, landform (1, valley bottom; 2, draw or slope of draw; 3, ridge). Aspect: 1, south west; 2, south or west; 3, north west or south east; 4, north; 5, north east), slope, wet (wet class 1–5: increases with the distance from mountain to ravine), pH, P, available phosphorus; TP, total phosphorus; N, available nitrogen; TN, total nitrogen; SOM, organic matter; K, available potassium.

significant difference can be seen in pH (Mann–Whitney U = 0.00, P < 0.001), available phosphorus (Mann–Whitney U = 0.00, P < 0.001), total phosphorus (Mann–Whitney U = 0.00, P < 0.001), available nitrogen (Mann–Whitney U = 0.00, P < 0.001), total nitrogen (Mann–Whitney U = 0.00, P < 0.001), and available potassium (Mann–Whitney U = 0.00, P < 0.001), while the differences in organic matter were not significant (Mann–Whitney U = 25.5, P < 0.859).

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The relations between functional groups and environmental factors were studied on the basis of the relative basal area (Table 5). Functional group 1 was found to have positive correlations with factors such as pH (R = 0.98, P < 0.01), stone percentage (R = 0.88, P < 0.05), available K (R = 0.83, P < 0.05), total phosphorus (R = 0.85, P < 0.05) and the wet class (R = 0.80, P < 0.05) and a negative correlation with landform (R = 0.80, P < 0.05). This reflected the fact that ravine stands had such characteristics as higher stone content, pH, available potassium, total phosphorus and wet class, and were distributed mainly at lower elevations (R1 and R2). FG2 was found to have positive correlations with elevation (R = 0.93, P < 0.01), organic matter (R = 0.87, P < 0.05) and negative correlations with wet class (R = 0.97, P < 0.01), pH (R = 0.83, P < 0.05) and available potassium (R = 0.90, P < 0.01). This reflected mainly the fact that the mountain slope stands had such environmental characteristics as higher elevation, lower pH and, available potassium, and a drier climate (M1, M3 and M4). FG3 was found to have negative correlations with elevation (R = 0.91, P < 0.01), organic matter (R = 0.84, P < 0.05) and positive relations with the wet class (R = 0.83, P < 0.05) and available potassium (R = 0.82, P < 0.05). It mainly reflected that the ravine forest stands (R1 and R2) had environmental characteristics such as lower elevation, higher wet class and available potassium. FG4 was not correlated significantly with any environmental factor, but had weak positive relations with wet class and pH, and weak negative relations with elevation and organic matter. This reflected the differences in environmental characteristics between ravine stands and mountain slope stands, and was distributed mainly in the mountain slope stand M2, close to the ravine stands. FG5 and FG7 were not correlated significantly with any environmental factor. Both had weak positive relations with the wet class and pH, and a weak negative relation with organic matter. FG5 was distributed mainly in the ravine stands, while FG7 was distributed mainly in the ravine forest gaps.

Table 5 Correlations between environmental factors and tree functional groups based on relative basal area Correlations (abbreviation and unit)

FG1

FG2

FG3

FG4

FG5

FG6

FG7

FG8

Elevation (m) Landforma Aspectb Slope (8) Stone (%) Wet classc pH Available phosphorus (P, mg kg1) Total phosphorus (TP, mg kg1) Available nitrogen (N, mg kg1) Total nitrogen (TN, mg kg1) Organic matter (SOM, %) Available potassium (K, mg kg1)

0.65 0.80* 0.05 0.59 0.88* 0.80* 0.98** 0.05 0.85* 0.53 0.22 0.52 0.83*

0.93** 0.65 0.37 0.66 0.68 0.97** 0.83* 0.41 0.59 0.05 0.31 0.87* 0.90**

0.91** 0.64 0.13 0.26 0.58 0.83* 0.71 0.45 0.52 0.27 0.44 0.84* 0.82*

0.48 0.22 0.38 0.59 0.02 0.53 0.07 0.50 0.07 0.47 0.63 0.65 0.30

0.54 0.49 0.27 0.11 0.22 0.40 0.22 0.21 0.15 0.50 0.38 0.45 0.49

0.95** 0.34 0.03 0.18 0.35 0.75 0.59 0.76 0.30 0.46 0.70 0.95** 0.62

0.79 0.54 0.55 0.56 0.44 0.72 0.70 0.44 0.33 0.05 0.19 0.66 0.59

0.45 0.76 0.37 0.84* 0.85* 0.76 0.83* 0.23 0.78 0.64 0.42 0.32 0.80

Bold values are significance at P < 0.05; *P < 0.05, **P < 0.01. a Landform: 1, valley bottom; 2, draw or slope of draw; 3, ridge. b Aspect: 1, south west; 2, south or west; 3, north west or south east; 4, north; 5, north east. c The wet class: determined from the distance to ravine, decreases with the distance.

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FG6 and FG8 were not correlated significantly with any environmental factor, which reflected, in part, the environmental characteristics of mountain slope forest stands. FG6 was correlated positively with elevation (R = 0.95, P < 0.01) and organic matter (R = 0.95, P < 0.01). FG8 was correlated negatively with landform (R = 0.84, P < 0.05), stone content (R = 0.85, P < 0.05), pH (R = 0.83, P < 0.05) and available K (R = 0.80, P < 0.05). 3. Discussion The tropical forests on Hainan Island are rich in species diversity. Functional group analysis is an effective way to study and analyze the ecosystem dynamics and functions of tropical forests. This study combined several methods to find the key functional traits for species classification in identifying the functional groups in this old-growth tropical montane rain forest and understand their relations with different aspects of the environment. The procedures of functional group identification might be extended to other species-rich plant communities. 3.1. Selection of the functional traits A tropical forest has highly diverse species and a heterogeneous environment that make it difficult to test the functional traits and ecological process of every species accurately. In many studies, functional group identification is based on observable plant functional traits that reflect seed dispersal, regeneration, growth and reproduction (Denslow, 1996; Metzger, 2000; Michalski et al., 2007; Poorter et al., 2006; Swaine and Whitmore, 1988; ter Steege et al., 2006; Verburg and van Eijk-Bos, 2003). In this study, we selected seven functional traits (growth form, potential height, buttress size, leaf phenology, seed mass, dispersal agent and wood density) of plants as the basis for further quantitative classification of functional groups in the tropical montane rain forest. These plant functional traits are used widely, are easy to measure and can indicate important ecological functioning. For example, potential height is one of the most important factors in classification of tropical forest species (Clark and Clark, 1999). Potential height is related to species competitiveness, breeding capacity and the recovery time after disturbances such as fire, typhoon and logging. It is related directly to the spatial location of the species among the communities, its use of ecological resources and its position in the ecosystem (Turner, 1996). The buttress is an important feature of species in tropical forests. Different buttresses have different morphology and growth state, but they all have similar functions in providing structural support to its own load and against wind actions. For example, the sizes of the buttress of species in the canopy layer decreases with the decrease in canopy height (Richards, 1996). Wood density is closely related to some ecological factors, which can influence the growth of species in tropical forests. It is one of the important indicators of a species successional situation (ter Steege and Hammond, 2001). Defoliation is an important functional trait of forest communities, and a significant

indicator for plant classification, moisture status detection, and remote sensing monitoring of vegetation (Bohlman et al., 1998). Seed mass is important in functional group classification. It is a result of natural selection in the long interaction between the life history features and the environmental factors of the species (Westoby, 1992). Seed mass is closely related to factors such as light (Turner, 1990), moisture (Howe, 1990), nutritient availability (Foster et al., 1986), seed dispersal (Howe et al., 1985) and predators (Janzen, 1970). The adaptation of a species to certain seed dispersal agents can dictate regeneration speed and regeneration, and greatly influence the composition and abundance of animal communities in a region (Richards, 1996). 3.2. The relations between tree functional traits In this study, the key traits for functional group identification were buttress size, potential height and seed mass, and then wood density. Potential height was positively correlated with buttress size and seed mass, but was correlated only weakly with other functional traits. Seed mass was negatively correlated with wood density and seed dispersal agent. Falster and Westoby (2005) reported consistent results in the study of the relations between seed mass, wood density, leaf mass per area, stem mass, leaf mass, and leaf mass fraction. They proposed three reasons to explain the relations. (1) The strategic trade-offs between individual traits might be inherently loose (Poorter and Navas, 2003), at least compared with physically enforced relations (Westoby et al., 2002). (2) Height-related trade-offs accounted for variation in other traits only partly and additional factors such as hydrology or soil nutrients must also be accounted for. (3) It may be that the true relations were obscured, at least partially, by biases or limitations in their methods, because they had not explored other and perhaps more important factors such as phenotype and genotype. Our study indicated that potential height was significantly related to buttress, which agreed with other studies. The buttress of a tropical forest tree has long been thought to serve as a structural support, and has been viewed as a response to physiological stresses that could force aerial proliferation of shallow root systems or as mechanical adaptations to support a tree against asymmetrical loads (Ruchter, 1984), which result in growth of the most heavily stressed area near the trunk and result in the formation of a buttress (Mattheck and Kubler, 1995). The buttress becomes proportionately larger as the tree grows, providing the tree with greater support for its crown, which becomes exposed to the stronger winds of the upper forest canopy (Ruchter, 1984). Our study indicated that potential height was significantly correlated with seed mass. A tendency for larger species to have larger seeds has been recognized in other studies (Leishman et al., 2000; Moles et al., 2004). In the most comprehensive studies to date, seed size and maximum potential height were positively correlated across 2113 species from a wide range of habitats, including deserts, grasslands, shrublands, temperate and tropical forests. It is unclear why larger species tend to have larger fruits and seeds (Moles et al., 2004). Presumably,

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diaspore dispersal distance increases with plant height, at least for wind-assisted diaspores or for those without specialized dispersal adaptations. While this may contribute to the relations observed between plant height and seed mass, it does not provide a general explanation: these relations are actually just as strong among species with animal-dispersed diaspores as among those with wind-assisted or unassisted dispersal (Leishman et al., 2000). A promising recent explanation is based on the time taken to reach reproductive maturity (Moles et al., 2004). The argument is as follows (Moles et al., 2004): species that are large as adults have a long juvenile period, and to survive this requires high juvenile survivorship, which is associated with a large seed mass and hence there is a link between seed mass and plant size. It is similar to the positive relation between adult body size and offspring mass at the time of independence seen in mammals (Charnov, 1993), but a full test of these ideas would require quantification of the relation between seed mass and survival from seed production to reproductive maturity. Potential height was weakly related to wood density in our study. Gelder et al. (2006) indicated that maximum adult stature was not correlated with wood density or safety factors when all species were pooled. If species are classified into lightdemanding and shade-tolerant species, potential height and wood density are positively correlated (Sterck et al., 2001). Falster and Westoby (2005) showed that potential height alone cannot fully express a species’ strategy for light capture, because it does not distinguish the contrasting strategies in early versus late successional situations (Sterck et al., 2001). In tropical rain forests, light is thought to be the most limiting factor for plant growth and survival, and light availability increases horizontally from the understorey to gap centers, and vertically from the forest floor to the upper canopy. Short-lived and shade-tolerant species spend their whole lifetime under a closed forest canopy and have greater lifetime risks of being hit by falling debris. Therefore, they need denser, stronger and stiffer wood and more mechanical safety to survive in the understorey. Tall, shade-tolerant species, on the other hand, escape size-dependent damage. With their low wood density and low safety margins, they grow rapidly and efficiently to the upper canopy to attain their large reproductive size. Therefore, potential height is positively related to light, while negatively related to wood density (Falster and Westoby, 2005; Gelder et al., 2006). Short-lived pioneers dominate early in succession, where growth is fast and competition for light is strongest. They therefore have a low wood density and grow at low safety margins to escape competition with neighbors, but with the development of succession they will be substituted by tall pioneer species (Falster and Westoby, 2005; Gelder et al., 2006). These tall pioneer species are also often longer-lived and need to invest in denser, stronger, stiffer wood and mechanical safety to be able to persist for a long time in the closing canopy (Falster and Westoby, 2005; Gelder et al., 2006). Seed mass was negatively correlated with wood density in our study, probably because both traits can indicate the status of regenerative strategies (Grime et al., 1997). Species earlier in succession generally have small seed mass but with have large

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seed numbers and can occupy the growth space quickly, while the species in later succession have a large seed mass and have strong survivorship in low-light environments (Leishman et al., 1995). Our results showed that wood density was significantly correlated with deciduous versus evergreen species. Tropical tree defoliation is positively correlated with water shortage under conditions of lower precipitation and in the dry season, in which defoliation is extended (Reich, 1995). Wood density can indicate the drought-resistance of a species (Sperry, 2003). Species with low wood density tend to have highly conductive sapwood and store considerable water in their stems, while those with high wood density tend to be more resistant to xylem cavitation, and their leaves show larger daily fluctuations in leaf water potential (Ackerly, 2004). All these show that species with greater wood density are distributed mainly in droughtprone environments, which is consistent with the viewpoint that greater wood density can protect pipe when water decreases in wood. 3.3. The relations between functional group distributions and environmental factors There is a recognized relation between functional groups and climate, particularly on the global or biome scale (Box, 1996; Prentice et al., 1992). By studying the relations between different functional groups and environmental factors, we identified the main environmental factors influencing the distribution of species in the tropical montane rain forest on Hainan Island. The results showed that the ravine forest stands had a greater content of soil nutrients than the mountain slope forest stands, which is similar to the tropical montane forest and ravine forest in the Yunan Province of China as reported by Xue et al. (2003). Growth form is related to physical factors such as moisture, elevation and light conditions. Functional groups based on different growth forms respond to environmental conditions of the tropical forest in different ways (Ewel and Bigelow, 1996). Usually, trees and shrubs are more abundant in good drainage conditions (Ashton, 1967; Wyatt, 1960). In the present study, trees and shrubs were more abundant in mountain slope stands than in the ravine stands. The abundance of epiphytes and palms is significantly related to annual precipitation (Ewel and Bigelow, 1996), since drought is the main constraint to the growth of epiphytes and palms. The abundance of these species increases with the increase of annual precipitation (Medina, 1999). Palms are common in tropical wet forest and on bottomland suffering from long-term or short-term flood erosion. A forest with palms as the main species may form an environment with long-term flood erosion (Kahn and Granville, 1992), since palms can tolerate an environment short of oxygen. The trunks of palms have a great capacity for water storage, which can be used when water absorbed by the roots is insufficient (Holbrook and Sinclair, 1992). In this study, epiphytes and palms were closely related to moisture, stone and soil pH, which mainly reflect the features of a ravine forest environment.

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Lianas and herbs have significant correlation with the amount of light available (Ewel and Bigelow, 1996). Light is the main factor that affects the growth of lianas, similar to its effect on trees in tropical rain forests (Rollet, 1969). Gaps in the canopy facilitate the growth of lianas (Putz, 1984). Herbs are distributed mainly in natural or non-natural opening areas, along roads or in a valley. They are rarely seen in old-growth rain forests, usually being either scattered or absent (Richards, 1996). Large gaps in the forest or steep slopes tend to have abundant herbs (Richards, 1996). In this study, ravine forest stands R1 and mountain slope stands near the ravine had a greater abundance of lianas, possibly due to more forest gaps formed by trees falling in the ravine stands as the result of typhoon damage. Herbs were less abundant in old-growth tropical mountain slope forest stands than in the ravine stands. In this study, the functional groups with maximum potential height and buttress were distributed mainly in ravine forest stands, and were adapted to the relatively wet and stony environment. Typhoon and storm are the most serious natural disturbance on Hainan Island. Suffering from long-term erosion, the ravine is composed mainly of sandstone accumulation and lacks good soil structure. Since the rich soil nutrients and water are concentrated on the soil surface in tropical ravine forest stands, the roots of trees growing there are shallow, and fallen and broken trees are often seen. In order to survive flooding, a species must have rapid seedling growth. Condit et al. (1999) and Newbery et al. (1999) pointed out that for saplings, shrubs and canopy trees, the growth rate of a primary forest in a humid environment is at least 10 times greater than that in a dry environment; therefore, along with the increasing growth rate, plant size is increased (Clark and Clark, 1992). Many studies have shown that the roots of tropical trees are very shallow (less than 1–2 m), and roots in a wet environment are shallower than those in a dry environment (Webb, 1959). Since buttresses can serve as structural supports against asymmetrical loads, and are easy to form under conditions of high temperature and humidity, their growth has long been viewed as a response to mechanical actions (Fisher, 1982) or physiological stresses that could force aerial proliferation of shallow root systems (Hall et al., 1978). Therefore, the functional groups of the upper layer in the Hainan Island tropical ravine forest stands had buttresses that were larger than those of the lower layer in the ravine forest or those of any functional groups in the mountain slope forest. The functional group with greatest seed mass (FG2) was distributed mainly in mountain slope forest stands, which might be a response to the high elevation and low soil nutrient content. FG6 and FG8 constituted the lower layer species of the mountain slope forest, which had less seed mass than those of the upper layer, but greater than those of the lower layer of ravine forest stands. Similarly, Mabura Hill (Guyana) is characterized by its environmental stability, such as less earthquake, wind damage and human distribution, and its species tend to have a large seed mass as the result of long-term selection. In contrast, Manu (Peru) is continuously affected by heavy soil erosion and is frequently colonized by small-seeded pioneers that require large and exposed areas for successful establishment (Swietenia macrophylla) (Terborgh, 1990).

Seed mass is the result of selective pressures being applied directly or indirectly in a variety of ways. Direct pressures include the factors that are thought to constrain seed and seedling survival continuously over long ecological times. Seedling emerging from larger seeds often survive longer than those from smaller seeds under adverse conditions, such as high defoliation, low light (Howe et al., 1985), low soil moisture and nutrient limitation (Manga and Yadav, 1995). There is some evidence that plants from dry habitats tend to have larger seeds. Baker (1972) conducted a survey of 2490 species in California and showed a fairly consistently positive relation between seed size and dry conditions. It is thought that greater seed reserves might enable the seedlings to establish roots quickly, thereby exploiting a greater volume of soil for moisture than would otherwise be possible. Jurado and Westoby (1992) found that when seeds were deprived of nutrients, large-seeded seedlings generally survived longer than small-seeded seedlings. Similarly, in this study, in both the upper and the lower storey species in the forest, the functional groups of mountain slope forest stands had greater seed mass than those of ravine forest stands. However, seed mass within one area differs greatly, the upper storey species of the forest have greater seed mass than the lower storey. That is because complex natural selective pressures and genetic attributes commonly have effects on seed mass; plant size and growth form have the greatest influences (Westoby, 1992). So, seed mass can vary greatly within one area or under different conditions of soil moisture or nutrients. In a survey of dunes in Indiana, Mazer (1989) was not able to show any significant relation between seed mass and water availability. Jurado and Westoby (1992), in a test involving Australian species, found that seedlings from heavier-seeded species did not (as they hypothesized) allocate a greater proportion of their resources to roots than lighter-seeded species. Leishman and Westoby (1994) suggested an advantage of larger seeds in dry soil, but field experiments failed to confirm this. Therefore, seed mass is the result of complex interactions between environmental selective pressures and genetic traits (1999). Seed mass is not the result of selection alone, but is influenced largely by plant traits such as potential height and growth form (Kelly, 1995). More detailed studies are needed to understand the mechanism. In conclusion, in the tropical montane rain forest on Hainan Island, the ravine stands were composed mainly of functional groups with the largest buttress and the greatest potential height, while the mountain slope stands at a higher elevation were composed mainly of functional groups with the greatest seed mass. The functional groups composed of species with the largest buttress and maximum potential height or greatest seed mass in the main layer of the forest (FG1 and FG2) were related most closely to environmental factors; and functional groups in the lower layer of the forest composed of species with larger buttress or greater seed mass (FG5, FG6 and FG8) can indicate environmental factors to a certain extent, but are less significant than those in the main layer of the forest (FG1 and FG2). However, functional groups composed of species with a smaller buttress, lower potential height or less seed mass in the main

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