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Testing the importance of native plants in facilitation the restoration of coastal plant communities dominated by exotics
Forest Ecology and Management 322 (2014) 19–26
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Testing the importance of native plants in facilitation the restoration of coastal plant communities dominated by exotics Xianzhao Liu a,b, Yuanchang Lu a,⇑, Yang Xue c, Xiongqing Zhang d a
Research Institute of Forest Resource Information Techniques, Chinese Academy of Forestry, Beijing 100091, PR China Key Laboratory for Silviculture and Conservation of Ministry of Education, Beijing Forestry University, Beijing 10091, PR China c Laboratory of Ecological Research, Forestry Science Institute, Hainan 571100, PR China d Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, PR China b
a r t i c l e
i n f o
Article history: Received 13 September 2013 Received in revised form 8 March 2014 Accepted 11 March 2014
Keywords: Interaction Leaf area index Aboveground biomass Biodiversity Understory dynamic Soil conditions
a b s t r a c t Casuarina equisetifolia was introduced to China in 1897 from Australia to reduce coastal erosion. It grows vigorously and has spread over much of the southern and southeastern coast, from Zhejiang to Guangxi, over a range of more than 10° of latitude. To date, little is known about its interactions with native species in the coastal zone. We used a field experiment to study how the understorey species diversity and soil conditions in monoculture stands of C. equisetifolia were influenced by different native plant species. We also examined the effects of interplanting native species on plant numbers, leaf area index (LAI), and aboveground biomass accumulation. We planted three native species (Hibiscus tiliaceus, Melia azedarach and Calophyllum inophyllum) at two initial densities in stands of C. equisetifolia. Over a period of ten years, the density and aboveground biomass were relatively low in plots planted with three native species compared to plots that were not planted. In contrast, understory diversity and soil conditions were relatively high where native species were added. Moreover, the number of dead tree, aboveground biomass increment, and diameter growth had significant difference among different native tree species because of their different natural characteristics. The fast-growing pioneer species, M. azedarach, had a positive effect on LAI, regeneration, shrub diversity and grass coverage than the other two native species, and M. azedarach was most effective in plots that were initially planted with higher densities. The pioneer plant H. tiliaceus had more individuals and greater aboveground biomass than others native species. The later-succession species C. inophyllum had the smallest effect on the development of understory vegetation and soil conditions over 10-yrs among three native plants. For different native planted species, M. azedarach showed good effects on the average annual aboveground biomass and DBH increment, and C. inophyllum had the least dead number in coastal environments. In summary, C. equisetifolia and native species have facilitation relationships that differ according to the species, and coastal conservation managers should shift from their traditional focus on C. equisetifolia afforestation to the recognition of multi-species configuration. Ó 2014 Published by Elsevier B.V.
1. Introduction Native species are those that have evolved over geological time in response to physical and biotic processes that are characteristic of a particular region; these characteristics include the climate, soil, timing of rainfall, drought, and interactions with other species in the local community (Richards et al., 1998; Palmer et al., 2003; ⇑ Corresponding author. Tel.: +86 10 62888448; fax: +86 10 62888315. E-mail addresses: [email protected] (X. Liu), [email protected] [email protected] (Y. Xue), [email protected] (X. Zhang). http://dx.doi.org/10.1016/j.foreco.2014.03.020 0378-1127/Ó 2014 Published by Elsevier B.V.
(Y.
Lu),
Callaway, 2007). These interactions shape the structure and function of communities and ecosystems (Wootton and Emmerson, 2005), affecting population growth and fecundity, abundance, geographical range, soil nutrient supply, community diversity and stability (Paige and Whitham, 1987; Maron, 1998; Novak and Wootton, 2010). Facilitation has long been recognised as a regulator of community organisation and as one of the most important positive community interactions (Bertness and Callaway, 1994; He et al., 2012). Facilitation also has applications to community restoration in harsh ecosystems (Brady et al., 2002). Because facilitation by exotic species is still debated (Simberloff and Von Holle,
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X. Liu et al. / Forest Ecology and Management 322 (2014) 19–26
1999; Rodriguez, 2006), the majority of experimental and theoretical research on facilitation focuses on native species, even if the interactions are between native and exotic species (Losos et al., 1993; Bezemer et al., 2006; Zhang et al., 2012). Exotic plants can change the composition and function of microbial communities, alter soil food web structures and influence nutrient cycling (Scharfy et al., 2010). These effects may arise from differences between native and exotic species in functional traits and allow exotic species to colonise and flourish in a habitat. Communities of invasive may be helpful in vegetation restoration, especially when the original community has been destroyed, but they are not usually the desired vegetation for the long term. To change the conditions of exotic-dominated communities, one promising approach is to find appropriate native species (or species groups) and use facilitation to adjust the structure and function of the current community. Casuarina equisetifolia, native to the southern and eastern coasts of Australia, was introduced to Hainan Island China to reduce coastal erosion in the 1950s, and immediately became the dominant species due to its pioneer characteristics, including fast growth, adaptability to barren soils, and ability to resist wind (Hammerton, 2001). C. equisetifolia has special canopy characters such as whorls of tiny scales, fine cladodes and tower-shaped morphological structure. These phenotypic traits increase wind resistance and allow better growth in hostile coastal environments (Chen et al., 2005). However, due to its high tannin content, the branches and leaves of C. equisetifolia decompose slowly, which decreases the speed of nutrient return and influences the growth of forest. The litter beneath C. equisetifolia (made up of fallen cladodes) can build up to form thick continuous deposits, which simply by their presence smother other species and prevent establishment (Hammerton, 2001; Batish et al., 2001). In addition, machine-cultivated afforestation with monocultures of C. equisetifolia was once the sole management approach for protecting coastal forests and this approach destroyed the composition and structure of the original community along with the soil seed bank, causing native species to disappear from reforested lands. As a result, forest productivity declined and forest succession in the tropical coastal zone was arrested by the lack of native species (Wheeler et al., 2011). To change above conditions, three native tree species (see Table 1 – Hibiscus tiliaceus, Melia azedarach and Calophyllum inophyllum) that once thrived in the coastal forest were interplanted with one-year-old C. equisetifolia in the monoculture. Comparing the response by such native species to their shared neighbours can reduce the harmful effects of C. equisetifolia and help develop management strategies for native species. In this study, we examine the effects through which these native species have interacted with C. equisetifolia during 10-yrs of succession in the tropical coast of southern China. Our general objective is to understand whether an exotic forest community can be changed by other native species. The specific objectives of this study were to determine: (1) how the understorey species diversity and soil conditions in monoculture stands of C. equisetifolia were influenced by different native species; (2) how the effects of different mixed afforestation on dynamics of planted species (number, LAI and biomass accumulation) as the forest developed.
2. Materials and methods 2.1. Site description and experimental design The study was conducted in the northeast coastal zone of Hainan Island, adjacent to the South China Sea, in the monsoon tropics of south China (Fig. 1). Soils were coastal sand with the following general particle size distribution:>1.0 mm: 6.15%; 1.0–0.5 mm: 10.23%; 0.5–0.25 mm: 27.17%; 0.25–0.1 mm: 53.63%; <0.1 mm: 2.82%. The soil structure was loose, with good permeability but low water-retention properties. The organic matter content (<0.15%) and nutrient elements were also low. The tropical marine climate ensures rainfall of 1720 mm annually and temperatures (over 24-hour) averaging 22–24 °C. We initiated the experiment to examine the effects of planting native tree species (Table 1) along with C. equisetifolia on the process of tropical coastal forest succession and habitat restoration. We employed 7 planting levels: C. equisetifolia only, H. tiliaceus I, H. tiliaceus II, M. azedarach I, M. azedarach II, C. inophyllum I and C. inophyllum II (I indicates that the proportion of C. equisetifolia to native species is 1:1, a II indicates a ratio of 2:1). The experimental treatments were determined using a randomised block design with three blocks. Each block contained one replicate (20 20 m2) of each planting level (Fig. 1). Within each plot, one subplots of 5 5 m2 were placed to survey species recruitment. For each plot, we investigated the number, LAI, the DBH (diameter at breast height) and height of planted species; for each subplot, we investigated composition and number of natural regeneration and shrub; moreover, the grass coverage and soil conditions (pH value, organic matter and total nitrogen) were also investigated in each subplot. All items were investigated every two years (2000, 2002, 2004, 2006, 2008, and 2010) with the exception of soil nutrient (only 2000 and 2010). The initial density of afforestation was 2500 stems per hectare (100 per plot). With time, the number of trees in each plot was changed because of factors such as typhoon, self-thinning, competition and herbivory.
2.2. Dynamics of planted species Each species has a survival strategy for a hostile environment. In every experimental plot, the number of trees per hectare of planted species was recorded biennially (2000–2010) to document survival in the various experimental plantings. Moreover, the number difference of dead trees among treatments and tree species were also recorded at the same time. Relative to other parts of a tree, the crown is always impacted most by the windy climate in a coastal zone. LAI the one-sided green leaf area per unit ground surface, was used to assess the canopy condition in the plots. Canopy photographs were taken in every plot in the vertical direction (Nikon + Fisheye lens) in late August, and the LAI index was obtained by a canopy analysis system from the photographs (Hemiview 2.1, Delta-T Devices Ltd., Cambridge, Britain). Biomass, in ecology, is the mass of living biological organisms in a given area or ecosystem at a given time and is closely correlated with stand volume in forest surveys. Biennially (2000–2010), the
Table 1 Natural characteristics of three native tree species. Species
H. tiliaceus M. azedarach C. inophyllum
Family
Malvaceae Meliaceae Guttiferae
Succession stage
Pioneer Pioneer Later
Tolerance Shade
Barren
Wind
Medium Low Medium
High High Medium
High Low Medium
Growth
Body size
Litter
Middle Fast Slow
Small Big Big
Medium Heavy Little
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X. Liu et al. / Forest Ecology and Management 322 (2014) 19–26
The South China Sea China A B C
Wenchang city Hainan province
Fig. 1. Study sites in the northeast coastal zone, near Wenchang city, Hainan Province, China. A, B, and C indicate three experiment blocks (2 hm2 16 each). Seven planting treatment plots were placed in each block. All sites are influenced by the maritime climate. The light gray area in the top right corner indicates the distribution of C. equisetifolia in China.
DBH and height of planted individuals were measured in every experimental plot of 400 m2. Then, the two parameters were used to calculate aboveground biomass using four biomass equations from the literature (Rana et al., 2001; Li and Lei, 2010): 2
0:503
2
0:993386
C: equisetifolia : Y ¼ 0:776468ðd HÞ
M: azedarach : Y ¼ 0:0278601ðd HÞ 2
H: tiliaceus : Y ¼ 0:0495502ðd HÞ 2
C: inophyllum : Y ¼ 0:044ðd HÞ
0:952453
0:9169
ð1Þ ð2Þ ð3Þ ð4Þ
where the Y is the individual above-ground biomass (kg), d is the DBH (cm), and H is the tree height (m). As growth and productivity are important items for forest management, the DBH growth and biomass increment per unit were also checked through analysing the measured tree diameter and calculated aboveground biomass every two years. 2.3. Understory vegetation performance Litter from C. equisetifolia has a low decompose capacity and impedes the germination of understory plants, despite the relative openness of the canopy and ample rainfall (Hammerton, 2001). In our study, recruitment was recorded in every experimental plot in two permanent subplots of 25 m2. For each plot, the results from the subplots were used to calculate the number of trees per hectare, the diversity of trees and shrub (use Shannon-Wiener index [H0 ].) and grass coverage. All of these measurements were taken in late November biennially (from 2000 to 2010).
2.4. Soil condition Poor soil nutrient availability is a main factor in the vegetation growth of C. equisetifolia coastal forest. Facilitating litter decomposition may be an important management option, but significant barriers to litter decomposition must be overcome (Hammerton, 2001). In our study, soil samples were collected for nutrient analysis from the different planting levels to evaluate the role of native species on soil condition. Baseline soil data were collected in 2000 along with other surveys. Three punch-tube samples of the upper 15 cm of sandy soil were collected and mixed together for every plot. These bulk samples were then analysed for total N by micro-Kjeldahl, for soil acidity using the pH of water at a 1:2.5 soil/water ratio, and total organic matter by a modified Walkley–Black procedure (Page et al., 1982). Because the change in soil conditions was slow, a 2nd survey was taken in 2010.
2.5. Statistical analysis All data were first checked for normality and homogeneity of variance by non-parametric test and chi-square test, and results showed that all data obeying normal distribution and homogeneity of variance. We then analysed data using planting treatment (7 levels) as fixed and block (3 levels) as random effects. Measurements that were repeated in different years were analysed using a repeated-measures analysis of variance (RANOVA). This analysis takes into account the overall treatment effect, independent of time, as well as the within-treatment effect of whether treatments respond differently over time. The seven planting levels were then compared using a Tukey test based on the overall effect (independent of time). Moreover, the variation of soil elements in the different planting levels was analysed and compared using a one-way
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ANOVA and a Tukey test. All of the data were analysed using SPSS 11.0 (Statistic Package for Social Science see NorusI, 2002).
3. Results 3.1. Dynamics of planted species Plots planted with C. equisetifolia had significantly more individuals (2020 N/hm2) than other treatments (Table 2; Appendix A). The average number (planted species) was not significantly different when the initial mixed proportion was II during the 10-yrs (Fig. 2A: H. tiliaceus II [1975 stems/hm2], C. inophyllum II [1969 stems/hm2], and M. azedarach II [1947 stems/hm2]). In contrast, the average number of above species fell significantly when the initial proportion was I (Fig. 2A: H. tiliaceus [1916 stems/ hm2], C. inophyllum [1872 stems/hm2], and M. azedarach [1840 stems/hm2]). The number of native dead tree per hectare had significant difference among six mixed planting treatments (F5,10 = 14.71; P < 0.001) during 10-yr. C. inophyllum had the largest dead number (642 stems/hm2) when the mixed proportion was I (Table 3), next was M. azedarach I (567 stems/hm2) and H. tiliaceus I (517 stems/ hm2). H. tiliaceus II had the least number of native dead trees (400 stems/hm2). For the same native tree species, the number of dead trees in treatments which the mixed proportion was I were higher than mixed proportion II (Table 3). On the contrary, the number of exotic dead trees (C. equisetifolia) had no significant difference among six mixed planting treatments (Table 3; F5,10 = 0.911; P = 0.506), which indicated the death of exotic trees had little relationship with different planting treatments. LAI were significantly different at the 7 planting levels (F = 336.10, P < 0.001). The average LAI in plots planted with M. azedarach II was significantly higher (LAI = 1.31) than plots with other planting levels (Fig. 2B). M. azedarach I had the second highest LAI (1.27). The LAI in plots planted with only C. equisetifolia was significantly higher (1.22) than LAI in the other four planting levels, which included H. tiliaceus and C. inophyllum. The differences between H. tiliaceus–C. equisetifolia and C. inophyllum–C. equisetifolia were not significant when they were mixed in the same proportion. The aboveground biomass was, on average, highest in plots with no native species planted (C. equisetifolia monoculture: 64.64 t/hm2). The plots that included the native species H. tiliaceus (55.80 t/hm2) or M. azedarach (54.19 t/hm2) at the proportion II had more biomass than the other two pairs. Biomass in mixed plots of C. inophyllum I was lowest (42.32) because the species grows very slowly. For the difference of native species characteristics (Table 1), the average annual aboveground biomass increment of native trees species had significant difference among six mixed planting treatments (F5,10 = 113.26; P < 0.001). As a fast-growing species,
M. azedarach had the largest annual aboveground biomass increment (4.43 t/hm2a) in the treatment of M. azedarach I during 10-yr period, next was M. azedarach in the treatment of M. azedarach II (2.47 t/hm2 a), C. inophyllum had the least annual aboveground biomass increment (0.46 t/hm2 a) in the treatment of C. inophyllum II. For the same native tree species, the annual aboveground biomass increment per hectare in treatments which the mixed proportion was I were higher than mixed proportion II (Table 3). The annual aboveground biomass increment of exotic tree species also had significant difference among seven planting treatments (F6,12 = 94.28; P < 0.001), C. equisetifolia had largest annual aboveground biomass increment per hectare (16.33 t/hm2 a) among all planting treatments. Unlike native tree species, aboveground biomass increment of C. equisetifolia in treatments which the mixed proportion was I were lower than mixed proportion II (Table 3). The mean annual DBH growth of native plant species had significant difference among six mixed planting treatments (F5,10 = 57.94; P < 0.001). M. azedarach had the largest annual DBH growth (0.93 cm/a) in the treatment of M. azedarach I (Table 3), next was M. azedarach in the treatment of M. azedarach II (0.86 cm/a). The significant differences of DBH growth of native tree species among six mixed afforestation treatments were main influenced by species characteristics (Table 1). For the same native tree species, the difference of mean annual DBH growth between mixed proportion I and II was not significant (Table 3). The mean annual DBH growth of exotic plant species had significant difference among seven planting treatments (F6,12 = 4.704; P = 0.008), C. equisetifolia in the treatment of H. tiliaceus I had the largest annual DBH growth (1.08 cm/a), while had the lowest annual DBH growth (0.97 cm/a) in the treatment of M. azedarach II (Table 3). 3.2. Understory vegetation performance The abundance and diversity of natural regenerating saplings differed significantly among the 7 treatments (Table 2). The average abundance (2578 N/hm2) and diversity (H0 : 1.02) in plots of M. azedarach I was significantly higher than other treatments. Next was the M. azedarach II, with a number and diversity (H0 ) of 1766 N/hm2 and 0.81. For the other two native species, the abundance and diversity in plots mixed with C. equisetifolia at proportion I were higher than proportion II. The plot planted with C. inophyllum had higher recruitment of native species than H. tiliaceus. The abundance (1066 N/hm2) and diversity (0.28) in pure C. equisetifolia plots was lowest (Fig. 2D and E). The plots originally planted with M. azedarach I had the highest shrub diversity (H’: 1.23) of the 7 treatments, and next were C. inophyllum I and H. tiliaceus I, which had the second and third diversity values, respectively (Fig. 2F). The shrub diversity in plots planted only with C. equisetifolia was lowest (0.63), and the gap
Table 2 Plant characteristics (mean ± SE) for different stands growing in plots with seven planting treatments over a 10-yr period. Planting treatments
The number of trees per hectare (stems/hm2)
LAI
Aboveground biomass of planted species (t/hm2)
The number of regeneration tree per hectare (stems/hm2)
Shannon–Wiener index (H0 ) (Regeneration species)
Shannon–Wiener index (H0 ) (shrub species)
Grass abundance (%)
H. tiliaceus I H. tiliaceus II M. azedarach I M. azedarach II C. inophyllum I C. inophyllum II C. equisetifolia
1916c ± 36 1975b ± 20 1840e ± 48 1947b ± 25 1872d ± 24 1969b ± 18 2020a ± 16
1.07f ± 0.02 1.13e ± 0.01 1.27b ± 0.01 1.31a ± 0.01 1.06f ± 0.02 1.14de ± 0.01 1.22c ± 0.02
43.59d ± 2.86 55.80b ± 1.58 52.98c ± 1.53 54.19bc ± 0.92 42.32d ± 1.44 51.60c ± 1.29 64.64a ± 0.79
1678bc ± 99 1267c ± 84 2578a ± 148 1766b ± 101 1733b ± 117 1422bc ± 128 1066c ± 77
0.68c ± 0.06 0.59c ± 0.07 1.02a ± 0.09 0.81b ± 0.10 0.64c ± 0.08 0.54c ± 0.06 0.28d ± 0.05
0.93b ± 0.10 0.73cd ± 0.10 1.23a ± 0.13 0.90bc ± 0.10 0.98b ± 0.16 0.84c ± 0.12 0.63d ± 0.07
30ab ± 3 24b ± 2 32a ± 2 27b ± 2 30ab ± 3 26b ± 2 18c ± 2
Within rows, means followed by different letters are significant differences (P < 0.05) based on a Tukey’s hsd test following the overall effect analysis of RANOVA.
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X. Liu et al. / Forest Ecology and Management 322 (2014) 19–26 1.8
2400
A
B 1.6
Leaf Area Index (LAI)
No. plant species (n/hm2)
2200
2000
1800
1600
1.0
H.tiliaceus I H.tiliaceus II M. azedarach I M. azedarach II C. inophyllum I C. inophyllum II C. equisetifolia
0.6 2000
2002
2004
2006
2008
2010
2000
2002
2004
2006
2008
2010
6000
200
D
C
5000
No. recruitment species (n/hm2)
160
Aboveground biomass (t/hm2)
1.2
0.8
1400
180
1.4
140 120 100 80 60 40
4000
3000
2000
1000
20 0 2000
2002
2004
2006
2008
0 2000
2010
2.0
2.0
1.5
1.0
.5
0.0 2000
2004
2006
2008
2010
2002
2004
2006
2008
2010
F
1.5
Diversity of shrub species
Diversity of regeneration species
E
2002
1.0
.5
0.0 2002
2004
2006
2008
2010
2000
Fig. 2. Plant species/hm2, leaf area index (LAI), aboveground biomass, recruitment of native tree species/hm2, and diversity of regeneration and shrubs (mean SE, n = 3) in plots with different planting treatments for the years 2000–2010.
(0.60) in the most diverse group of shrub was lower than the regeneration diversity (gap: 0.74). Grass cover differed significantly between treatment groups, though only for M. azedarach I and the C. equisetifolia monoculture
(Table 2). The cover of grass increased sharply in 2008, averaging more than 50% relative to previous surveys, and then it dropped slowly through 2010. The species list of the understory vegetation is in Appendix B.
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Table 3 Number of dead trees, growth of DBH and aboveground biomass (mean ± SE) in plots with seven planting treatments over a 10-yr period.
H. tiliaceus I H. tiliaceus II M. azedarach I M. azedarach II C. inophyllum I C. inophyllum II C. equisetifolia
Mean number of native dead plants (stems/hm2)
Mean number of dead exotic plants (stems/hm2)
Mean DBH growth of native plant (cm/a)
Mean DBH growth of exotic plant (cm/a)
Mean aboveground biomass increment of native plant (t/hm2 a)
Mean aboveground biomass increment of exotic plant (t/hm2 a)
517b ± 36 400c ± 14 567ab ± 22 433bc ± 22 642a ± 8 450bc ± 29 –
442a ± 30 442a ± 22 392a ± 22 425a ± 14 417a ± 8 442a ± 22 –
0.71b ± 0.02 0.68b ± 0.01 0.86a ± 0.02 0.93a ± 0.05 0.48c ± 0.01 0.66c ± 0.01 –
1.08a ± 0.008 1.06a ± 0.004 1.03ab ± 0.023 0.97b ± 0.062 1.05ab ± 0.223 1.02ab ± 0.223 1.00ab ± 0.004
1.01c ± 0.05 0.54c ± 0.02 4.43a ± 0.58 2.47b ± 0.16 0.84c ± 0.08 0.46c ± 0.08 –
9.78d ± 0.53 13.96b ± 0.32 9.04d ± 0.20 12.31c ± 0.47 9.24d ± 0.10 12.70bc ± 0.24 16.33a ± 0.22
Within rows, means followed by different letters are significant differences (P < 0.05) based on ANOVA and Tukey post-hoc test.
3.3. Soil conditions The 10-yr of site occupancy by tree plantations significantly altered many soil properties, but the various treatments affected soils very differently. The average soil pH in the plots planted with C. equisetifolia only, was significantly higher than it was in the other treatments (8.87), followed by C. inophyllum II (Table 4; Appendix C). The rest of the treatments could again be divided into three grades according to the results of multiple comparisons. Treatments of C. inophyllum I, H. tiliaceus II and H. tiliaceus I were in the first group. Their average soil pH values were 8.43, 8.30 and 8.17, respectively. Soil pH in plots planted with M. azedarach I (7.78) and II (8.03) were in the last grade, they were significantly lower than other treatments. They also decreased significantly during the 10-yr period, which was nearly twice the change as was created in the H. tiliaceus I and II plots, and nearly 5 times greater than in the plots of C. inophyllum I and II or in the C. equisetifolia monoculture (Table 4). The change of soil pH in the C. equisetifolia treatment was significantly lower than in the other treatments during the 10-yr period (Table 4; Appendix C). Soil organic matter (OM), on average, was significantly different among the seven treatments (F6,12 = 98.85; P < 0.01). Plots planted with M. azedarach I had the highest soil organic matter (0.58%) in all treatments. Soil OM in plots planted with H. tiliaceus was higher than that of C. inophyllum. For each type of native species, soil OM in plots with proportion I were significantly higher than proportion II at the 0.05 level, but the difference was not significant at the 0.01 level. Average soil OM in the C. equisetifolia treatment was lowest (0.375%), although it was not significantly different from C. inophyllum II. The variation in soil organic matter was not the same at different planting levels during the 10-yr period. Soil organic matter increased significantly beneath M. azedarach I (0.10%) and II (0.06%), and beneath H. tiliaceus I (0.06%), but decreased significantly beneath C. equisetifolia (0.09%), C. inophyllum I (0.03%) and H. tiliaceus II (0.03%). Soil organic matter in plots planted with H. tiliaceus II also increased (0.02%), but not significantly (Table 4; Appendix C).
The average totals of N in plots planted with M. azedarach (I: [0.82 g/kg] and II: [0.79 g/kg]) were significantly higher than those of the other 5 planting treatments (Table 4). H. tiliaceus and C. inophyllum had the next highest total N. The plot planted only with C. equisetifolia had the lowest soil total N (0.39 g/kg). The total N increased significantly over the study period beneath the treatment of M. azedarach (II: [0.27 g/kg] and I: [0.24 g/kg]), and those values were clearly higher than other treatments (Table 4; Appendix C). The variation of total N in the plots planted with only C. equisetifolia (0.09 g/kg) changed the least.
4. Discussion Species always perform better in their native communities, even if some species are absent. Gleason (1917) argued that the functional characteristics of species within communities, rather than diversity per se, are the most important drivers of plant community composition and the greatest influence on community assemblage and development. Foresters seldom use native species to change the structure and condition of communities of invasives, leaving them dominant and allowing them to hinder alternative succession processes. Our study shows that the facilitation between native- and exotic- species can improve such communities over a ten year time frame. Moreover, we posit that in addition to direct interactions between planted species, the influences of native species in facilitating diversity, richness and better soil conditions can contribute to habitat restoration. Our results thus support the hypothesis that the initial assemblage of a plant community is crucial in determining the composition of a plant community in the longer term (Bezemer et al., 2006), even if that assemblage is dominated by an exotic species. Species respond differently to environmental stress, and their strategies are changed by interspecific interactions in multispecies assemblages. Compared with C. inophyllum and H. tiliaceus, M. azedarach seedlings do very poorly in the open, but their recruitment improves under C. equisetifolia, which provides shelter against a harsh maritime environment. Our study shows that the
Table 4 Soil pH, organic matter and total N (mean ± SE) in the upper 15 cm of soil after 10 yrs of site occupancy by different plant species. Soil organic matter (g kg1)
Soil pH
H. tiliaceus I H. tiliaceus II M. azedarach I M. azedarach II C. inophyllum I C. inophyllum II C. equisetifolia
Soil total N (g kg1)
2000
2010
Change
2000
2010
Change
2000
2010
Change
8.70 ± 0.10 8.77 ± 0.15 8.37 ± 0.06 8.47 ± 0.06 8.70 ± 0.10 8.87 ± 0.06 8.97 ± 0.06
8.17 ± 0.06 8.30 ± 0.10 7.20 ± 0.10 7.60 ± 0.10 8.43 ± 0.06 8.67 ± 0.06 8.77 ± 0.06
0.53c 0.47cd 1.17a 0.87b 0.27d 0.2d 0.2d
0.47 ± 0.01 0.45 ± 0.01 0.53 ± 0.02 0.51 ± 0.02 0.44 ± 0.01 0.40 ± 0.03 0.42 ± 0.05
0.53 ± 0.01 0.47 ± 0.01 0.63 ± 0.04 0.57 ± 0.02 0.41 ± 0.01 0.37 ± 0.01 0.33 ± 0.03
0.06bc 0.02c 0.10a 0.06b 0.03cd -0.03d -0.09e
0.19 ± 0.01 0.17 ± 0.01 0.29 ± 0.03 0.26 ± 0.01 0.18 ± 0.01 0.17 ± 0.01 0.15 ± 0.01
0.39 ± 0.02 0.34 ± 0.02 0.53 ± 0.02 0.53 ± 0.02 0.34 ± 0.01 0.31 ± 0.02 0.24 ± 0.01
0.2b 0.17bc 0.24ab 0.27a 0.16bc 0.14c 0.09d
Within rows, means followed by different letters are significant differences (P < 0.05) based on ANOVA and Tukey post-hoc test.
X. Liu et al. / Forest Ecology and Management 322 (2014) 19–26
number of alive individuals in each treatment has positive correlation with the initial density of C. equisetifolia during 10-yr period. For the same native tree species, the number of dead trees in treatments with more C. equisetifolia individuals (proportion II) were higher than the other (proportion I). While, the death of exotic trees had little relationship with different planting treatments. H. tiliaceus can take full advantage of the protective effect from C. equisetifolia, and had higher survivorship than the other two species during the 10-yr period. The crown canopy always undergoes more stress in coastal environments, and special canopy characters allow C. equisetifolia to maintain a stable canopy condition and higher LAI even in harsh surroundings. As a fast-growing species, M. azedarach raises the stand LAI more than other two native species. The effects on LAI by M. azedarach are negligible. There was a big drop of LAI in 2008 in all plots (Fig. 2B), this might be caused by the fierce typhoon activity in the survey interval (between 2006 and 2008). Beyond any maximum-yield density, interactions occur as component species strive to capture resources from a shared location (Jose et al., 2006). Relative to C. inophyllum and H. tiliaceus, M. azedarach has more capacity to accumulate biomass because it grows quickly, although this does not improve the biomass accumulation in the mixed forest because of the resource competition from C. equisetifolia. Although the effect of H. tiliaceus on biomass accumulation is small, the resource utilisation between H. tiliaceus and C. equisetifolia is less competitive, raising their total aboveground biomass accumulation when planted together (Tables 2 and 3). The mean DBH growth of native tree species were mainly depend on their characteristic. For those exotic trees, the mean DBH growth were not only depend on the type of native species but on initial mixed proportion (Table 3). In understory, shrubs play an important role in ecosystems because they are resistant to climate conditions, especially to drought or a saline environment (Aich, 1991). Natural regeneration also plays a key role on vegetation restoration and development. In our experiment, native species planted at different densities with C. equisetifolia influenced the understory characteristics such as diversity and grass abundance. All of the understory layers (regeneration, shrub, and grass) were improved in the M. azedarach treatments (I and II), followed by H. tiliaceus (I and II). Although C. inophyllum treatments (I and II) had less effect than the other two native species, it still provided a marginal improvement over the monoculture of C. equisetifolia. For each native species, understory vegetation improved more under level I than II. However, we provide no direct evidence to explain the role of native species on recruitment, regeneration and shrub development. Nevertheless, the development of different species assemblages can profoundly affect understory vegetation dynamics and produce results such as those of Bezemer et al. (2006). Many earlier studies have been performed on short time scales and used artificial management (such as weeding) (Van Ruijven et al., 2003; Meiners et al., 2004). Therefore, data on the influence of different species configurations on understory vegetation restoration in the absence of human interference over 10-yrs are meaningful for coastal vegetation management. Land rehabilitation through reestablishment of native trees is becoming increasingly attractive because native trees have been shown to improve soil conditions significantly on badly degraded tropical l and (Fisher, 1995). Soil pH is considered a master variable in soils as it controls many chemical processes. It specifically affects plant nutrient availability by controlling the chemical forms of the nutrients. McTlwee and NeSmith (1971) indicated that the optimum pH range for most plants is between 5.5 and 7.0. Although many plants have adapted to thrive at pH values outside of this range, very high soil pH values strongly influence the ‘‘boom and bust’’ development of coastal plant communities. Our study
25
shows that planting native species, especially M. azedarach, lowers the soil pH even when mixed with C. equisetifolia. For each native species, soil pH decreased more in level I than level II. Soil organic matter is the main source of nutrients for plant growth and soil development, and it can improve soil physical properties and accelerate the activities of microorganisms (Bot and Benites, 2005). Because C. equisetifolia litter decomposes very slowly, the organic matter content is low and easily lost in a coastal sandy soils (Wheeler et al., 2011). In our experiment, the soil organic matter increases significantly in plots planted with M. azedarach and C. equisetifolia over 10-yrs. H. tiliaceus had a lesser effect, but was still able to increase the soil OM. Although soil OM declined in plots planted with C. inophyllum (I and II), but the decrement was significantly less than that of the C. equisetifolia stand. Although the species used in our study are not nitrogen-fixing plant, native species (M. azedarach especially) effectively increased the soil total N when interplanted with the nitrogen-fixing plant C. equisetifolia. These changes in soil conditions might result from litter effects or the recruitment of understory vegetation, but this hypothesis has not yet to be confirmed. 5. Conclusions Complexity of community structure, species richness and diversity, and soil fertility are the main factors in forest vegetation dynamics (Palmer et al., 2003; Knapp, 1974). Plant facilitation can play an important role in these factors and may promote early succession in abandoned fields (Bertness and Leonard, 1997; Van der Putten et al., 2000; Halpern et al., 2007). We used a 10-yr experiment on species configuration to show how native species change a community dominated by C. equisetifolia. As a fastgrowing pioneer species, M. azedarach showed better effects on the development of both stands (aboveground biomass, species diversity, etc.) and soil conditions (organic matter, total N, etc.) when mixed with C. equisetifolia. Moreover, other two latersuccessional species (H. tiliaceus and C. inophyllum) could also improve the quality of C. equisetifolia in the monoculture. Our results indicate that managing the native species assembly could solve some of the problems caused by species such as C. equisetifolia, change the structure and function of coastal forest ecosystems and promote the process of forest succession. Acknowledgements This study was funded by the State Forestry Bureau research and public service industry (201004002, 201304320) and the China Postdoctoral Science Foundation (2012M510331). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foreco.2014.03. 020. References Aich, A.E., 1991. Role of shrubs in ecosystem functions. CIHEAM – Opt. Mediterr. 16, 43–46. Batish, D.R., Singh, H.P., Kohli, R.K., 2001. Vegetation exclusion under Casuarina equisetifolia L.: does allelopathy play a role? Commun. Ecol. 2, 93–100. Bertness, M.D., Callaway, R., 1994. Positive interactions in communities. Trends Ecol. Evol. 9, 191–193. Bertness, M.D., Leonard, G.H., 1997. The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78, 1976–1989. Bezemer, T.M., Harvey, J.A., Kowalchuk, G.A., Korpershoek, H., Van Der Putten, W.H., 2006. Interplay between Senecio Jacobaea and plant, soil, and aboveground insect community composition. Ecology 87, 2002–2013.
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Bot, A., Benites, J., 2005. The importance of soil organic matter. FAO Soil Bulletin, Food and Agriculture Organization of the Unired Nations, Rome, Italy, p. 1–4. Brady, V.J., Cardinale, B.J., Gathman, J.P., 2002. Does facilitation of faunal recruitment benefit ecosystem restoration? An experimental study of invertebrate assemblages in wetland mesocosms. Restore Ecol. 10, 617–626. Callaway, R.M., 2007. Positive interactions and interdependence in plant communities. Springer, The Netherlands Press, Dordrecht, 415p. Chen, Y., Wang, G.M., Zhou, J., 2005. Advances in the study of stress resistance of Casuarina equisetifolia. Chin. Bull. Bot. 22, 746–752 (in Chinese). Fisher, R.F., 1995. Amelioration of degraded rain forest soils by plantations of native trees. Soil Sci. Soc. Am. J. 59, 544–549. Gleason, H.A., 1917. The structure and development of the plant association. B Torrey Bot. Club 53, 7–26. Halpern, B.S., Silliman, B.R., Olden, J.D., Bruno, J.P., Bertness, M.D., 2007. Incorporating positive interactions in aquatic restoration and conservation. Front Ecol. Environ. 3, 153–160. Hammerton, J., 2001. Casuarinas in the Bahamas: a clear and present danger. Bahamas J. Sci. 9, 2–14. He, Q., Cui, B.S., Bertness, M.D., AN, Y., 2012. Testing the importance of plant strategies on facilitation using congeners in a coastal community. Ecology 93, 2023–2029. Jose, S., Williams, R., Zamora, D., 2006. Belowground ecological interactions in mixed species forest plantations. Forest Ecol. Manag. 233, 231–239. Knapp, R. (Ed.), 1974. Vegetation dynamic. Handbook of Vegetation Science, vol. 8. Dr. W. Junk bv, The Hague Press, 737p. Li, H.K., Lei, Y.C., 2010. Estimation and Evaluation of Forest Biomass Carbon Storage in China. China Forestry Publishing Press, Beijing, 60p. Losos, J.B., Marks, J.C., Schoener, T.W., 1993. Habitat use and ecological interactions of an introduced and a native species of Anolis lizard on Grand Cayman, with a review of outcomes of anole introductions. Oecologia 95, 525–532. Maron, J.L., 1998. Insect herbivory above-and belowground: individual and joint effects on plant fitness. Ecology 79, 1281–1293. McTlwee, E.W., NeSmith, J., 1971. Soil reaction (pH) for flowers, shrubs, and lawn around the home. Florida Coop. Exten. Service, 352. Meiners, S.J., Cadenasso, M.L., Pickett, S.T.A., 2004. Beyond biodiversity: individualistic controls of invasion in a self-assembled community. Ecol. Lett. 7, 121–126.
NorusI, M.J., 2002. SPSS 11.0 guide to data analysis. Prentice Hall, Upper Saddle River, NJ. Novak, M., Wootton, J.T., 2010. Using experimental indices to quantify the strength of species interactions. Oikos 119, 1057–1063. Page, A.L., Miller, R.H., Keeney, D.R. (Eds.), 1982. Methods of soil analysis. Part 2. second ed. Agrom. Monogr. 9. ASA and SSSA Madison, WI. Paige, K.N., Whitham, T.G., 1987. Overcompensation in response to mammalian herbivory the advantage of being eaten. Am. Natl. 129, 407–416. Palmer, T.M., Stanton, M.L., Young, T.P., 2003. Competition and coexistence: exploring mechanisms that restrict and maintain diversity within mutualist guilds. Am. Natl. 162, S63–S79. Rana, B.S., Rao, O.P., Singh, B.P., 2001. Biomass production in 7 year old plantations of Casuarina equisetifolia on sodic soil. Trop. Ecol. 2, 207–212. Richards, R.T., Chambers, J.C., Ross, C., 1998. Use of native plants on federal lands: policy and practice. J. Range Manage 6, 625–632. Rodriguez, L.R., 2006. Can invasive species facilitate native species? Evidence of how, when, and why these impacts occur. Biol. Invasions 8, 927–939. Scharfy, D., Guesewell, S., Gessner, M.O., Venterink, H.O., 2010. Invasion of Solidago gigantea in contrasting experimental plant communities: effects on soil microbes, nutrients and plant–soil feedbacks. J. Ecol. 98, 1379–1388. Simberloff, D., Von Holle, B., 1999. Positive interactions of nonindigenous species: invasional meltdown? Biol. Invasions 1, 21–32. Van der Putten, W.H., Mortimer, S.R., Hedlund, K., van Dijk, C., Brown, V.K., 2000. Plant species diversity as a driver of early succession in abandoned fields: a multi-site approach. Oecologia 124, 91–99. Van Ruijven, J., De Deyn, G.B., Berendse, F., 2003. Diversity reduces invasibility in experimental plant communities: the role of plant species. Ecol. Lett. 6, 910– 918. Wheeler, G.S., Taylor, G.S., Gaskin, J.F., Purcell, M.F., 2011. Ecology and management of sheoak (Casuarina spp.), an invader of coastal Florida, U.S.A. J. Coastal Res. 3, 485–492. Wootton, J.T., Emmerson, M., 2005. Measurement of interaction strength in nature. Annu. Rev. Ecol. Evol. Syst. 36, 419–444. Zhang, Y.H., Huang, G.M., Wang, W.Q., Chen, L.Z., Lin, G.H., 2012. Interactions between mangroves and exotic Spartina in an authropogenically disturbed estuary in southern China. Ecology 93, 588–597.
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Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco
Testing the importance of native plants in facilitation the restoration of coastal plant communities dominated by exotics Xianzhao Liu a,b, Yuanchang Lu a,⇑, Yang Xue c, Xiongqing Zhang d a
Research Institute of Forest Resource Information Techniques, Chinese Academy of Forestry, Beijing 100091, PR China Key Laboratory for Silviculture and Conservation of Ministry of Education, Beijing Forestry University, Beijing 10091, PR China c Laboratory of Ecological Research, Forestry Science Institute, Hainan 571100, PR China d Research Institute of Forestry, Chinese Academy of Forestry, Beijing 100091, PR China b
a r t i c l e
i n f o
Article history: Received 13 September 2013 Received in revised form 8 March 2014 Accepted 11 March 2014
Keywords: Interaction Leaf area index Aboveground biomass Biodiversity Understory dynamic Soil conditions
a b s t r a c t Casuarina equisetifolia was introduced to China in 1897 from Australia to reduce coastal erosion. It grows vigorously and has spread over much of the southern and southeastern coast, from Zhejiang to Guangxi, over a range of more than 10° of latitude. To date, little is known about its interactions with native species in the coastal zone. We used a field experiment to study how the understorey species diversity and soil conditions in monoculture stands of C. equisetifolia were influenced by different native plant species. We also examined the effects of interplanting native species on plant numbers, leaf area index (LAI), and aboveground biomass accumulation. We planted three native species (Hibiscus tiliaceus, Melia azedarach and Calophyllum inophyllum) at two initial densities in stands of C. equisetifolia. Over a period of ten years, the density and aboveground biomass were relatively low in plots planted with three native species compared to plots that were not planted. In contrast, understory diversity and soil conditions were relatively high where native species were added. Moreover, the number of dead tree, aboveground biomass increment, and diameter growth had significant difference among different native tree species because of their different natural characteristics. The fast-growing pioneer species, M. azedarach, had a positive effect on LAI, regeneration, shrub diversity and grass coverage than the other two native species, and M. azedarach was most effective in plots that were initially planted with higher densities. The pioneer plant H. tiliaceus had more individuals and greater aboveground biomass than others native species. The later-succession species C. inophyllum had the smallest effect on the development of understory vegetation and soil conditions over 10-yrs among three native plants. For different native planted species, M. azedarach showed good effects on the average annual aboveground biomass and DBH increment, and C. inophyllum had the least dead number in coastal environments. In summary, C. equisetifolia and native species have facilitation relationships that differ according to the species, and coastal conservation managers should shift from their traditional focus on C. equisetifolia afforestation to the recognition of multi-species configuration. Ó 2014 Published by Elsevier B.V.
1. Introduction Native species are those that have evolved over geological time in response to physical and biotic processes that are characteristic of a particular region; these characteristics include the climate, soil, timing of rainfall, drought, and interactions with other species in the local community (Richards et al., 1998; Palmer et al., 2003; ⇑ Corresponding author. Tel.: +86 10 62888448; fax: +86 10 62888315. E-mail addresses: [email protected] (X. Liu), [email protected] [email protected] (Y. Xue), [email protected] (X. Zhang). http://dx.doi.org/10.1016/j.foreco.2014.03.020 0378-1127/Ó 2014 Published by Elsevier B.V.
(Y.
Lu),
Callaway, 2007). These interactions shape the structure and function of communities and ecosystems (Wootton and Emmerson, 2005), affecting population growth and fecundity, abundance, geographical range, soil nutrient supply, community diversity and stability (Paige and Whitham, 1987; Maron, 1998; Novak and Wootton, 2010). Facilitation has long been recognised as a regulator of community organisation and as one of the most important positive community interactions (Bertness and Callaway, 1994; He et al., 2012). Facilitation also has applications to community restoration in harsh ecosystems (Brady et al., 2002). Because facilitation by exotic species is still debated (Simberloff and Von Holle,
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X. Liu et al. / Forest Ecology and Management 322 (2014) 19–26
1999; Rodriguez, 2006), the majority of experimental and theoretical research on facilitation focuses on native species, even if the interactions are between native and exotic species (Losos et al., 1993; Bezemer et al., 2006; Zhang et al., 2012). Exotic plants can change the composition and function of microbial communities, alter soil food web structures and influence nutrient cycling (Scharfy et al., 2010). These effects may arise from differences between native and exotic species in functional traits and allow exotic species to colonise and flourish in a habitat. Communities of invasive may be helpful in vegetation restoration, especially when the original community has been destroyed, but they are not usually the desired vegetation for the long term. To change the conditions of exotic-dominated communities, one promising approach is to find appropriate native species (or species groups) and use facilitation to adjust the structure and function of the current community. Casuarina equisetifolia, native to the southern and eastern coasts of Australia, was introduced to Hainan Island China to reduce coastal erosion in the 1950s, and immediately became the dominant species due to its pioneer characteristics, including fast growth, adaptability to barren soils, and ability to resist wind (Hammerton, 2001). C. equisetifolia has special canopy characters such as whorls of tiny scales, fine cladodes and tower-shaped morphological structure. These phenotypic traits increase wind resistance and allow better growth in hostile coastal environments (Chen et al., 2005). However, due to its high tannin content, the branches and leaves of C. equisetifolia decompose slowly, which decreases the speed of nutrient return and influences the growth of forest. The litter beneath C. equisetifolia (made up of fallen cladodes) can build up to form thick continuous deposits, which simply by their presence smother other species and prevent establishment (Hammerton, 2001; Batish et al., 2001). In addition, machine-cultivated afforestation with monocultures of C. equisetifolia was once the sole management approach for protecting coastal forests and this approach destroyed the composition and structure of the original community along with the soil seed bank, causing native species to disappear from reforested lands. As a result, forest productivity declined and forest succession in the tropical coastal zone was arrested by the lack of native species (Wheeler et al., 2011). To change above conditions, three native tree species (see Table 1 – Hibiscus tiliaceus, Melia azedarach and Calophyllum inophyllum) that once thrived in the coastal forest were interplanted with one-year-old C. equisetifolia in the monoculture. Comparing the response by such native species to their shared neighbours can reduce the harmful effects of C. equisetifolia and help develop management strategies for native species. In this study, we examine the effects through which these native species have interacted with C. equisetifolia during 10-yrs of succession in the tropical coast of southern China. Our general objective is to understand whether an exotic forest community can be changed by other native species. The specific objectives of this study were to determine: (1) how the understorey species diversity and soil conditions in monoculture stands of C. equisetifolia were influenced by different native species; (2) how the effects of different mixed afforestation on dynamics of planted species (number, LAI and biomass accumulation) as the forest developed.
2. Materials and methods 2.1. Site description and experimental design The study was conducted in the northeast coastal zone of Hainan Island, adjacent to the South China Sea, in the monsoon tropics of south China (Fig. 1). Soils were coastal sand with the following general particle size distribution:>1.0 mm: 6.15%; 1.0–0.5 mm: 10.23%; 0.5–0.25 mm: 27.17%; 0.25–0.1 mm: 53.63%; <0.1 mm: 2.82%. The soil structure was loose, with good permeability but low water-retention properties. The organic matter content (<0.15%) and nutrient elements were also low. The tropical marine climate ensures rainfall of 1720 mm annually and temperatures (over 24-hour) averaging 22–24 °C. We initiated the experiment to examine the effects of planting native tree species (Table 1) along with C. equisetifolia on the process of tropical coastal forest succession and habitat restoration. We employed 7 planting levels: C. equisetifolia only, H. tiliaceus I, H. tiliaceus II, M. azedarach I, M. azedarach II, C. inophyllum I and C. inophyllum II (I indicates that the proportion of C. equisetifolia to native species is 1:1, a II indicates a ratio of 2:1). The experimental treatments were determined using a randomised block design with three blocks. Each block contained one replicate (20 20 m2) of each planting level (Fig. 1). Within each plot, one subplots of 5 5 m2 were placed to survey species recruitment. For each plot, we investigated the number, LAI, the DBH (diameter at breast height) and height of planted species; for each subplot, we investigated composition and number of natural regeneration and shrub; moreover, the grass coverage and soil conditions (pH value, organic matter and total nitrogen) were also investigated in each subplot. All items were investigated every two years (2000, 2002, 2004, 2006, 2008, and 2010) with the exception of soil nutrient (only 2000 and 2010). The initial density of afforestation was 2500 stems per hectare (100 per plot). With time, the number of trees in each plot was changed because of factors such as typhoon, self-thinning, competition and herbivory.
2.2. Dynamics of planted species Each species has a survival strategy for a hostile environment. In every experimental plot, the number of trees per hectare of planted species was recorded biennially (2000–2010) to document survival in the various experimental plantings. Moreover, the number difference of dead trees among treatments and tree species were also recorded at the same time. Relative to other parts of a tree, the crown is always impacted most by the windy climate in a coastal zone. LAI the one-sided green leaf area per unit ground surface, was used to assess the canopy condition in the plots. Canopy photographs were taken in every plot in the vertical direction (Nikon + Fisheye lens) in late August, and the LAI index was obtained by a canopy analysis system from the photographs (Hemiview 2.1, Delta-T Devices Ltd., Cambridge, Britain). Biomass, in ecology, is the mass of living biological organisms in a given area or ecosystem at a given time and is closely correlated with stand volume in forest surveys. Biennially (2000–2010), the
Table 1 Natural characteristics of three native tree species. Species
H. tiliaceus M. azedarach C. inophyllum
Family
Malvaceae Meliaceae Guttiferae
Succession stage
Pioneer Pioneer Later
Tolerance Shade
Barren
Wind
Medium Low Medium
High High Medium
High Low Medium
Growth
Body size
Litter
Middle Fast Slow
Small Big Big
Medium Heavy Little
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The South China Sea China A B C
Wenchang city Hainan province
Fig. 1. Study sites in the northeast coastal zone, near Wenchang city, Hainan Province, China. A, B, and C indicate three experiment blocks (2 hm2 16 each). Seven planting treatment plots were placed in each block. All sites are influenced by the maritime climate. The light gray area in the top right corner indicates the distribution of C. equisetifolia in China.
DBH and height of planted individuals were measured in every experimental plot of 400 m2. Then, the two parameters were used to calculate aboveground biomass using four biomass equations from the literature (Rana et al., 2001; Li and Lei, 2010): 2
0:503
2
0:993386
C: equisetifolia : Y ¼ 0:776468ðd HÞ
M: azedarach : Y ¼ 0:0278601ðd HÞ 2
H: tiliaceus : Y ¼ 0:0495502ðd HÞ 2
C: inophyllum : Y ¼ 0:044ðd HÞ
0:952453
0:9169
ð1Þ ð2Þ ð3Þ ð4Þ
where the Y is the individual above-ground biomass (kg), d is the DBH (cm), and H is the tree height (m). As growth and productivity are important items for forest management, the DBH growth and biomass increment per unit were also checked through analysing the measured tree diameter and calculated aboveground biomass every two years. 2.3. Understory vegetation performance Litter from C. equisetifolia has a low decompose capacity and impedes the germination of understory plants, despite the relative openness of the canopy and ample rainfall (Hammerton, 2001). In our study, recruitment was recorded in every experimental plot in two permanent subplots of 25 m2. For each plot, the results from the subplots were used to calculate the number of trees per hectare, the diversity of trees and shrub (use Shannon-Wiener index [H0 ].) and grass coverage. All of these measurements were taken in late November biennially (from 2000 to 2010).
2.4. Soil condition Poor soil nutrient availability is a main factor in the vegetation growth of C. equisetifolia coastal forest. Facilitating litter decomposition may be an important management option, but significant barriers to litter decomposition must be overcome (Hammerton, 2001). In our study, soil samples were collected for nutrient analysis from the different planting levels to evaluate the role of native species on soil condition. Baseline soil data were collected in 2000 along with other surveys. Three punch-tube samples of the upper 15 cm of sandy soil were collected and mixed together for every plot. These bulk samples were then analysed for total N by micro-Kjeldahl, for soil acidity using the pH of water at a 1:2.5 soil/water ratio, and total organic matter by a modified Walkley–Black procedure (Page et al., 1982). Because the change in soil conditions was slow, a 2nd survey was taken in 2010.
2.5. Statistical analysis All data were first checked for normality and homogeneity of variance by non-parametric test and chi-square test, and results showed that all data obeying normal distribution and homogeneity of variance. We then analysed data using planting treatment (7 levels) as fixed and block (3 levels) as random effects. Measurements that were repeated in different years were analysed using a repeated-measures analysis of variance (RANOVA). This analysis takes into account the overall treatment effect, independent of time, as well as the within-treatment effect of whether treatments respond differently over time. The seven planting levels were then compared using a Tukey test based on the overall effect (independent of time). Moreover, the variation of soil elements in the different planting levels was analysed and compared using a one-way
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ANOVA and a Tukey test. All of the data were analysed using SPSS 11.0 (Statistic Package for Social Science see NorusI, 2002).
3. Results 3.1. Dynamics of planted species Plots planted with C. equisetifolia had significantly more individuals (2020 N/hm2) than other treatments (Table 2; Appendix A). The average number (planted species) was not significantly different when the initial mixed proportion was II during the 10-yrs (Fig. 2A: H. tiliaceus II [1975 stems/hm2], C. inophyllum II [1969 stems/hm2], and M. azedarach II [1947 stems/hm2]). In contrast, the average number of above species fell significantly when the initial proportion was I (Fig. 2A: H. tiliaceus [1916 stems/ hm2], C. inophyllum [1872 stems/hm2], and M. azedarach [1840 stems/hm2]). The number of native dead tree per hectare had significant difference among six mixed planting treatments (F5,10 = 14.71; P < 0.001) during 10-yr. C. inophyllum had the largest dead number (642 stems/hm2) when the mixed proportion was I (Table 3), next was M. azedarach I (567 stems/hm2) and H. tiliaceus I (517 stems/ hm2). H. tiliaceus II had the least number of native dead trees (400 stems/hm2). For the same native tree species, the number of dead trees in treatments which the mixed proportion was I were higher than mixed proportion II (Table 3). On the contrary, the number of exotic dead trees (C. equisetifolia) had no significant difference among six mixed planting treatments (Table 3; F5,10 = 0.911; P = 0.506), which indicated the death of exotic trees had little relationship with different planting treatments. LAI were significantly different at the 7 planting levels (F = 336.10, P < 0.001). The average LAI in plots planted with M. azedarach II was significantly higher (LAI = 1.31) than plots with other planting levels (Fig. 2B). M. azedarach I had the second highest LAI (1.27). The LAI in plots planted with only C. equisetifolia was significantly higher (1.22) than LAI in the other four planting levels, which included H. tiliaceus and C. inophyllum. The differences between H. tiliaceus–C. equisetifolia and C. inophyllum–C. equisetifolia were not significant when they were mixed in the same proportion. The aboveground biomass was, on average, highest in plots with no native species planted (C. equisetifolia monoculture: 64.64 t/hm2). The plots that included the native species H. tiliaceus (55.80 t/hm2) or M. azedarach (54.19 t/hm2) at the proportion II had more biomass than the other two pairs. Biomass in mixed plots of C. inophyllum I was lowest (42.32) because the species grows very slowly. For the difference of native species characteristics (Table 1), the average annual aboveground biomass increment of native trees species had significant difference among six mixed planting treatments (F5,10 = 113.26; P < 0.001). As a fast-growing species,
M. azedarach had the largest annual aboveground biomass increment (4.43 t/hm2a) in the treatment of M. azedarach I during 10-yr period, next was M. azedarach in the treatment of M. azedarach II (2.47 t/hm2 a), C. inophyllum had the least annual aboveground biomass increment (0.46 t/hm2 a) in the treatment of C. inophyllum II. For the same native tree species, the annual aboveground biomass increment per hectare in treatments which the mixed proportion was I were higher than mixed proportion II (Table 3). The annual aboveground biomass increment of exotic tree species also had significant difference among seven planting treatments (F6,12 = 94.28; P < 0.001), C. equisetifolia had largest annual aboveground biomass increment per hectare (16.33 t/hm2 a) among all planting treatments. Unlike native tree species, aboveground biomass increment of C. equisetifolia in treatments which the mixed proportion was I were lower than mixed proportion II (Table 3). The mean annual DBH growth of native plant species had significant difference among six mixed planting treatments (F5,10 = 57.94; P < 0.001). M. azedarach had the largest annual DBH growth (0.93 cm/a) in the treatment of M. azedarach I (Table 3), next was M. azedarach in the treatment of M. azedarach II (0.86 cm/a). The significant differences of DBH growth of native tree species among six mixed afforestation treatments were main influenced by species characteristics (Table 1). For the same native tree species, the difference of mean annual DBH growth between mixed proportion I and II was not significant (Table 3). The mean annual DBH growth of exotic plant species had significant difference among seven planting treatments (F6,12 = 4.704; P = 0.008), C. equisetifolia in the treatment of H. tiliaceus I had the largest annual DBH growth (1.08 cm/a), while had the lowest annual DBH growth (0.97 cm/a) in the treatment of M. azedarach II (Table 3). 3.2. Understory vegetation performance The abundance and diversity of natural regenerating saplings differed significantly among the 7 treatments (Table 2). The average abundance (2578 N/hm2) and diversity (H0 : 1.02) in plots of M. azedarach I was significantly higher than other treatments. Next was the M. azedarach II, with a number and diversity (H0 ) of 1766 N/hm2 and 0.81. For the other two native species, the abundance and diversity in plots mixed with C. equisetifolia at proportion I were higher than proportion II. The plot planted with C. inophyllum had higher recruitment of native species than H. tiliaceus. The abundance (1066 N/hm2) and diversity (0.28) in pure C. equisetifolia plots was lowest (Fig. 2D and E). The plots originally planted with M. azedarach I had the highest shrub diversity (H’: 1.23) of the 7 treatments, and next were C. inophyllum I and H. tiliaceus I, which had the second and third diversity values, respectively (Fig. 2F). The shrub diversity in plots planted only with C. equisetifolia was lowest (0.63), and the gap
Table 2 Plant characteristics (mean ± SE) for different stands growing in plots with seven planting treatments over a 10-yr period. Planting treatments
The number of trees per hectare (stems/hm2)
LAI
Aboveground biomass of planted species (t/hm2)
The number of regeneration tree per hectare (stems/hm2)
Shannon–Wiener index (H0 ) (Regeneration species)
Shannon–Wiener index (H0 ) (shrub species)
Grass abundance (%)
H. tiliaceus I H. tiliaceus II M. azedarach I M. azedarach II C. inophyllum I C. inophyllum II C. equisetifolia
1916c ± 36 1975b ± 20 1840e ± 48 1947b ± 25 1872d ± 24 1969b ± 18 2020a ± 16
1.07f ± 0.02 1.13e ± 0.01 1.27b ± 0.01 1.31a ± 0.01 1.06f ± 0.02 1.14de ± 0.01 1.22c ± 0.02
43.59d ± 2.86 55.80b ± 1.58 52.98c ± 1.53 54.19bc ± 0.92 42.32d ± 1.44 51.60c ± 1.29 64.64a ± 0.79
1678bc ± 99 1267c ± 84 2578a ± 148 1766b ± 101 1733b ± 117 1422bc ± 128 1066c ± 77
0.68c ± 0.06 0.59c ± 0.07 1.02a ± 0.09 0.81b ± 0.10 0.64c ± 0.08 0.54c ± 0.06 0.28d ± 0.05
0.93b ± 0.10 0.73cd ± 0.10 1.23a ± 0.13 0.90bc ± 0.10 0.98b ± 0.16 0.84c ± 0.12 0.63d ± 0.07
30ab ± 3 24b ± 2 32a ± 2 27b ± 2 30ab ± 3 26b ± 2 18c ± 2
Within rows, means followed by different letters are significant differences (P < 0.05) based on a Tukey’s hsd test following the overall effect analysis of RANOVA.
23
X. Liu et al. / Forest Ecology and Management 322 (2014) 19–26 1.8
2400
A
B 1.6
Leaf Area Index (LAI)
No. plant species (n/hm2)
2200
2000
1800
1600
1.0
H.tiliaceus I H.tiliaceus II M. azedarach I M. azedarach II C. inophyllum I C. inophyllum II C. equisetifolia
0.6 2000
2002
2004
2006
2008
2010
2000
2002
2004
2006
2008
2010
6000
200
D
C
5000
No. recruitment species (n/hm2)
160
Aboveground biomass (t/hm2)
1.2
0.8
1400
180
1.4
140 120 100 80 60 40
4000
3000
2000
1000
20 0 2000
2002
2004
2006
2008
0 2000
2010
2.0
2.0
1.5
1.0
.5
0.0 2000
2004
2006
2008
2010
2002
2004
2006
2008
2010
F
1.5
Diversity of shrub species
Diversity of regeneration species
E
2002
1.0
.5
0.0 2002
2004
2006
2008
2010
2000
Fig. 2. Plant species/hm2, leaf area index (LAI), aboveground biomass, recruitment of native tree species/hm2, and diversity of regeneration and shrubs (mean SE, n = 3) in plots with different planting treatments for the years 2000–2010.
(0.60) in the most diverse group of shrub was lower than the regeneration diversity (gap: 0.74). Grass cover differed significantly between treatment groups, though only for M. azedarach I and the C. equisetifolia monoculture
(Table 2). The cover of grass increased sharply in 2008, averaging more than 50% relative to previous surveys, and then it dropped slowly through 2010. The species list of the understory vegetation is in Appendix B.
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X. Liu et al. / Forest Ecology and Management 322 (2014) 19–26
Table 3 Number of dead trees, growth of DBH and aboveground biomass (mean ± SE) in plots with seven planting treatments over a 10-yr period.
H. tiliaceus I H. tiliaceus II M. azedarach I M. azedarach II C. inophyllum I C. inophyllum II C. equisetifolia
Mean number of native dead plants (stems/hm2)
Mean number of dead exotic plants (stems/hm2)
Mean DBH growth of native plant (cm/a)
Mean DBH growth of exotic plant (cm/a)
Mean aboveground biomass increment of native plant (t/hm2 a)
Mean aboveground biomass increment of exotic plant (t/hm2 a)
517b ± 36 400c ± 14 567ab ± 22 433bc ± 22 642a ± 8 450bc ± 29 –
442a ± 30 442a ± 22 392a ± 22 425a ± 14 417a ± 8 442a ± 22 –
0.71b ± 0.02 0.68b ± 0.01 0.86a ± 0.02 0.93a ± 0.05 0.48c ± 0.01 0.66c ± 0.01 –
1.08a ± 0.008 1.06a ± 0.004 1.03ab ± 0.023 0.97b ± 0.062 1.05ab ± 0.223 1.02ab ± 0.223 1.00ab ± 0.004
1.01c ± 0.05 0.54c ± 0.02 4.43a ± 0.58 2.47b ± 0.16 0.84c ± 0.08 0.46c ± 0.08 –
9.78d ± 0.53 13.96b ± 0.32 9.04d ± 0.20 12.31c ± 0.47 9.24d ± 0.10 12.70bc ± 0.24 16.33a ± 0.22
Within rows, means followed by different letters are significant differences (P < 0.05) based on ANOVA and Tukey post-hoc test.
3.3. Soil conditions The 10-yr of site occupancy by tree plantations significantly altered many soil properties, but the various treatments affected soils very differently. The average soil pH in the plots planted with C. equisetifolia only, was significantly higher than it was in the other treatments (8.87), followed by C. inophyllum II (Table 4; Appendix C). The rest of the treatments could again be divided into three grades according to the results of multiple comparisons. Treatments of C. inophyllum I, H. tiliaceus II and H. tiliaceus I were in the first group. Their average soil pH values were 8.43, 8.30 and 8.17, respectively. Soil pH in plots planted with M. azedarach I (7.78) and II (8.03) were in the last grade, they were significantly lower than other treatments. They also decreased significantly during the 10-yr period, which was nearly twice the change as was created in the H. tiliaceus I and II plots, and nearly 5 times greater than in the plots of C. inophyllum I and II or in the C. equisetifolia monoculture (Table 4). The change of soil pH in the C. equisetifolia treatment was significantly lower than in the other treatments during the 10-yr period (Table 4; Appendix C). Soil organic matter (OM), on average, was significantly different among the seven treatments (F6,12 = 98.85; P < 0.01). Plots planted with M. azedarach I had the highest soil organic matter (0.58%) in all treatments. Soil OM in plots planted with H. tiliaceus was higher than that of C. inophyllum. For each type of native species, soil OM in plots with proportion I were significantly higher than proportion II at the 0.05 level, but the difference was not significant at the 0.01 level. Average soil OM in the C. equisetifolia treatment was lowest (0.375%), although it was not significantly different from C. inophyllum II. The variation in soil organic matter was not the same at different planting levels during the 10-yr period. Soil organic matter increased significantly beneath M. azedarach I (0.10%) and II (0.06%), and beneath H. tiliaceus I (0.06%), but decreased significantly beneath C. equisetifolia (0.09%), C. inophyllum I (0.03%) and H. tiliaceus II (0.03%). Soil organic matter in plots planted with H. tiliaceus II also increased (0.02%), but not significantly (Table 4; Appendix C).
The average totals of N in plots planted with M. azedarach (I: [0.82 g/kg] and II: [0.79 g/kg]) were significantly higher than those of the other 5 planting treatments (Table 4). H. tiliaceus and C. inophyllum had the next highest total N. The plot planted only with C. equisetifolia had the lowest soil total N (0.39 g/kg). The total N increased significantly over the study period beneath the treatment of M. azedarach (II: [0.27 g/kg] and I: [0.24 g/kg]), and those values were clearly higher than other treatments (Table 4; Appendix C). The variation of total N in the plots planted with only C. equisetifolia (0.09 g/kg) changed the least.
4. Discussion Species always perform better in their native communities, even if some species are absent. Gleason (1917) argued that the functional characteristics of species within communities, rather than diversity per se, are the most important drivers of plant community composition and the greatest influence on community assemblage and development. Foresters seldom use native species to change the structure and condition of communities of invasives, leaving them dominant and allowing them to hinder alternative succession processes. Our study shows that the facilitation between native- and exotic- species can improve such communities over a ten year time frame. Moreover, we posit that in addition to direct interactions between planted species, the influences of native species in facilitating diversity, richness and better soil conditions can contribute to habitat restoration. Our results thus support the hypothesis that the initial assemblage of a plant community is crucial in determining the composition of a plant community in the longer term (Bezemer et al., 2006), even if that assemblage is dominated by an exotic species. Species respond differently to environmental stress, and their strategies are changed by interspecific interactions in multispecies assemblages. Compared with C. inophyllum and H. tiliaceus, M. azedarach seedlings do very poorly in the open, but their recruitment improves under C. equisetifolia, which provides shelter against a harsh maritime environment. Our study shows that the
Table 4 Soil pH, organic matter and total N (mean ± SE) in the upper 15 cm of soil after 10 yrs of site occupancy by different plant species. Soil organic matter (g kg1)
Soil pH
H. tiliaceus I H. tiliaceus II M. azedarach I M. azedarach II C. inophyllum I C. inophyllum II C. equisetifolia
Soil total N (g kg1)
2000
2010
Change
2000
2010
Change
2000
2010
Change
8.70 ± 0.10 8.77 ± 0.15 8.37 ± 0.06 8.47 ± 0.06 8.70 ± 0.10 8.87 ± 0.06 8.97 ± 0.06
8.17 ± 0.06 8.30 ± 0.10 7.20 ± 0.10 7.60 ± 0.10 8.43 ± 0.06 8.67 ± 0.06 8.77 ± 0.06
0.53c 0.47cd 1.17a 0.87b 0.27d 0.2d 0.2d
0.47 ± 0.01 0.45 ± 0.01 0.53 ± 0.02 0.51 ± 0.02 0.44 ± 0.01 0.40 ± 0.03 0.42 ± 0.05
0.53 ± 0.01 0.47 ± 0.01 0.63 ± 0.04 0.57 ± 0.02 0.41 ± 0.01 0.37 ± 0.01 0.33 ± 0.03
0.06bc 0.02c 0.10a 0.06b 0.03cd -0.03d -0.09e
0.19 ± 0.01 0.17 ± 0.01 0.29 ± 0.03 0.26 ± 0.01 0.18 ± 0.01 0.17 ± 0.01 0.15 ± 0.01
0.39 ± 0.02 0.34 ± 0.02 0.53 ± 0.02 0.53 ± 0.02 0.34 ± 0.01 0.31 ± 0.02 0.24 ± 0.01
0.2b 0.17bc 0.24ab 0.27a 0.16bc 0.14c 0.09d
Within rows, means followed by different letters are significant differences (P < 0.05) based on ANOVA and Tukey post-hoc test.
X. Liu et al. / Forest Ecology and Management 322 (2014) 19–26
number of alive individuals in each treatment has positive correlation with the initial density of C. equisetifolia during 10-yr period. For the same native tree species, the number of dead trees in treatments with more C. equisetifolia individuals (proportion II) were higher than the other (proportion I). While, the death of exotic trees had little relationship with different planting treatments. H. tiliaceus can take full advantage of the protective effect from C. equisetifolia, and had higher survivorship than the other two species during the 10-yr period. The crown canopy always undergoes more stress in coastal environments, and special canopy characters allow C. equisetifolia to maintain a stable canopy condition and higher LAI even in harsh surroundings. As a fast-growing species, M. azedarach raises the stand LAI more than other two native species. The effects on LAI by M. azedarach are negligible. There was a big drop of LAI in 2008 in all plots (Fig. 2B), this might be caused by the fierce typhoon activity in the survey interval (between 2006 and 2008). Beyond any maximum-yield density, interactions occur as component species strive to capture resources from a shared location (Jose et al., 2006). Relative to C. inophyllum and H. tiliaceus, M. azedarach has more capacity to accumulate biomass because it grows quickly, although this does not improve the biomass accumulation in the mixed forest because of the resource competition from C. equisetifolia. Although the effect of H. tiliaceus on biomass accumulation is small, the resource utilisation between H. tiliaceus and C. equisetifolia is less competitive, raising their total aboveground biomass accumulation when planted together (Tables 2 and 3). The mean DBH growth of native tree species were mainly depend on their characteristic. For those exotic trees, the mean DBH growth were not only depend on the type of native species but on initial mixed proportion (Table 3). In understory, shrubs play an important role in ecosystems because they are resistant to climate conditions, especially to drought or a saline environment (Aich, 1991). Natural regeneration also plays a key role on vegetation restoration and development. In our experiment, native species planted at different densities with C. equisetifolia influenced the understory characteristics such as diversity and grass abundance. All of the understory layers (regeneration, shrub, and grass) were improved in the M. azedarach treatments (I and II), followed by H. tiliaceus (I and II). Although C. inophyllum treatments (I and II) had less effect than the other two native species, it still provided a marginal improvement over the monoculture of C. equisetifolia. For each native species, understory vegetation improved more under level I than II. However, we provide no direct evidence to explain the role of native species on recruitment, regeneration and shrub development. Nevertheless, the development of different species assemblages can profoundly affect understory vegetation dynamics and produce results such as those of Bezemer et al. (2006). Many earlier studies have been performed on short time scales and used artificial management (such as weeding) (Van Ruijven et al., 2003; Meiners et al., 2004). Therefore, data on the influence of different species configurations on understory vegetation restoration in the absence of human interference over 10-yrs are meaningful for coastal vegetation management. Land rehabilitation through reestablishment of native trees is becoming increasingly attractive because native trees have been shown to improve soil conditions significantly on badly degraded tropical l and (Fisher, 1995). Soil pH is considered a master variable in soils as it controls many chemical processes. It specifically affects plant nutrient availability by controlling the chemical forms of the nutrients. McTlwee and NeSmith (1971) indicated that the optimum pH range for most plants is between 5.5 and 7.0. Although many plants have adapted to thrive at pH values outside of this range, very high soil pH values strongly influence the ‘‘boom and bust’’ development of coastal plant communities. Our study
25
shows that planting native species, especially M. azedarach, lowers the soil pH even when mixed with C. equisetifolia. For each native species, soil pH decreased more in level I than level II. Soil organic matter is the main source of nutrients for plant growth and soil development, and it can improve soil physical properties and accelerate the activities of microorganisms (Bot and Benites, 2005). Because C. equisetifolia litter decomposes very slowly, the organic matter content is low and easily lost in a coastal sandy soils (Wheeler et al., 2011). In our experiment, the soil organic matter increases significantly in plots planted with M. azedarach and C. equisetifolia over 10-yrs. H. tiliaceus had a lesser effect, but was still able to increase the soil OM. Although soil OM declined in plots planted with C. inophyllum (I and II), but the decrement was significantly less than that of the C. equisetifolia stand. Although the species used in our study are not nitrogen-fixing plant, native species (M. azedarach especially) effectively increased the soil total N when interplanted with the nitrogen-fixing plant C. equisetifolia. These changes in soil conditions might result from litter effects or the recruitment of understory vegetation, but this hypothesis has not yet to be confirmed. 5. Conclusions Complexity of community structure, species richness and diversity, and soil fertility are the main factors in forest vegetation dynamics (Palmer et al., 2003; Knapp, 1974). Plant facilitation can play an important role in these factors and may promote early succession in abandoned fields (Bertness and Leonard, 1997; Van der Putten et al., 2000; Halpern et al., 2007). We used a 10-yr experiment on species configuration to show how native species change a community dominated by C. equisetifolia. As a fastgrowing pioneer species, M. azedarach showed better effects on the development of both stands (aboveground biomass, species diversity, etc.) and soil conditions (organic matter, total N, etc.) when mixed with C. equisetifolia. Moreover, other two latersuccessional species (H. tiliaceus and C. inophyllum) could also improve the quality of C. equisetifolia in the monoculture. Our results indicate that managing the native species assembly could solve some of the problems caused by species such as C. equisetifolia, change the structure and function of coastal forest ecosystems and promote the process of forest succession. Acknowledgements This study was funded by the State Forestry Bureau research and public service industry (201004002, 201304320) and the China Postdoctoral Science Foundation (2012M510331). Appendix A. Supplementary material Supplementary data associated with this article can be found, in the online version, at http://dx.doi.org/10.1016/j.foreco.2014.03. 020. References Aich, A.E., 1991. Role of shrubs in ecosystem functions. CIHEAM – Opt. Mediterr. 16, 43–46. Batish, D.R., Singh, H.P., Kohli, R.K., 2001. Vegetation exclusion under Casuarina equisetifolia L.: does allelopathy play a role? Commun. Ecol. 2, 93–100. Bertness, M.D., Callaway, R., 1994. Positive interactions in communities. Trends Ecol. Evol. 9, 191–193. Bertness, M.D., Leonard, G.H., 1997. The role of positive interactions in communities: lessons from intertidal habitats. Ecology 78, 1976–1989. Bezemer, T.M., Harvey, J.A., Kowalchuk, G.A., Korpershoek, H., Van Der Putten, W.H., 2006. Interplay between Senecio Jacobaea and plant, soil, and aboveground insect community composition. Ecology 87, 2002–2013.
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