Effects of allelopathy and competition for water and nutrients on survival and growth of tree species in Eucalyptus urophylla plantations

Forest Ecology and Management 424 (2018) 387–395

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Effects of allelopathy and competition for water and nutrients on survival and growth of tree species in Eucalyptus urophylla plantations Fangcuo Qin, Shu Liu, Shixiao Yu

T

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Department of Ecology, School of Life Sciences/State Key Laboratory of Biocontrol, Sun Yat-sen University, Guangzhou 510275, China

A R T I C LE I N FO

A B S T R A C T

Keywords: Allelopathy Broad-leaved tree species Eucalyptus urophylla Resource competition

Allelopathy and resource competition are considered to be two primary mechanisms responsible for loss of biodiversity in plantations of Eucalyptus species. However, these two processes are usually studied separately, and they have been rarely tested on native woody species. In this study, we used a bioassay to assess sensitivities of twenty broad-leaved tree species on roots, stem growth and seed germination to leaf aqueous extracts of Eucalyptus urophylla S.T. Blake and categorized them into two types: inhibited and uninhibited (including stimulated and unaffected). To compare the relative importance of allelopathy and resource competition, we planted these two species groups into the E. urophylla plantation separately and treated with three gradients of irrigation-nutrients. The results showed that the allelopathic effects of aqueous extract of E. urophylla were species-specific and could be inhibitory, neutral or stimulatory. Compared to the inhibited species, the uninhibited species grew faster and survived better after they were planted in an E. urophylla plantation for approximately 10 years, suggesting that allelopathy from E. urophylla is an important restraining factor on native woody communities. Individuals from both species groups grew faster following higher resource treatment at the early but not the late stage of growth. Saplings did not vary in their survival rates across resource gradients. This indicates that resource competition between E. urophylla and native woody species has only a limited role in reducing the diversity of native species in an E. urophylla plantation. We conclude that allelopathy is more important than resource competition in mediating the reduction in plant biodiversity in E. urophylla plantations. Our study suggests that mixing certain types of species (e.g. Helicia cochinchinensis, Pterospermum lanceaefolium, Cinnamomum burmanni, Machilus chinensis, Acmena acuminatissima and Castanopsis chinensis) in E. urophylla plantations can mitigate against plant diversity loss.

1. Introduction Large scale plantations have been established by fast-growing tree species with the aim of producing timber for products such as paper, solid wood and firewood (Evans, 2009). Forestry plantations are typically characterised by densely planted monocultures of non-native trees. As a result, some native species have become endangered, and beneficial ecosystem services provided by native forests are diminishing (Foroughbakhch et al., 2001; Sangha and Jalota 2005). Eucalyptus, which belongs to Myrtaceae and native to Australia and South East Asia, is one of the fastest-growing and highest-yielding tree genera in tropical and subtropical areas (Zhao et al., 2007). Eucalyptus have been introduced into more than 120 countries, and they comprise one-third of the world’s total plantation area (Wu et al., 2015). There were 4.4 million ha of Eucalyptus plantation established in south China by the end of 2014 (Ou and Wang, 2015). However, the planting of Eucalyptus is still a controversial issue. Criticism is mainly focused on ⁎

the serious ecological problems caused by continuous planting of Eucalyptus in monoculture, such as soil degradation, increasing invasiveness and loss of understory biodiversity (Huang et al., 2007; Tang et al., 2013; Jin et al., 2015; Williams 2015). Studies have documented altered community composition (e.g. vegetation and soil microbial communities) in Eucalyptus plantations compared to other vegetated habitats (Proença et al., 2010; Calviño-Cancela et al., 2012; Wu et al., 2013). Reduction in biodiversity in Eucalyptus plantations is therefore a crucial issue for the long-term sustainability of native ecosystems (Tererai et al., 2013). Resource competition is an important mechanism which accounts for the adverse impact of Eucalyptus on native vegetation (Forsyth et al., 2004; Tererai et al., 2013). Eucalyptus plantations are often established on nutrient-poor bare ground, and because they are strongly competitive for soil nutrients and water, they may outcompete native species (Michelsen et al., 1996; Robinson et al., 2006; Neyland et al., 2009). Allelopathic effect is another important factor that has been blamed

Corresponding author at: Department of Ecology, School of Life Sciences, Sun Yat-sen University, Guangzhou 510275, China. E-mail address: [email protected] (S. Yu).

https://doi.org/10.1016/j.foreco.2018.05.017 Received 9 February 2018; Received in revised form 6 May 2018; Accepted 8 May 2018 0378-1127/ © 2018 Elsevier B.V. All rights reserved.

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2. Materials and methods

for the reduction of plant biodiversity in Eucalyptus plantations (May and Ash, 1990; Michelsen et al., 1996; Fang et al., 2009). Allelopathic effects have been studied extensively (Sasikumar et al., 2002; Bajwa and Nazi, 2005; El-Khawas and Shehata, 2005). In general, allelochemicals are released into the environment by volatilization, leaching, decomposition and excretion (Blum, 2011). Phenolic acids and volatile terpenes have been extracted from the leaves, bark and roots of Eucalyptus (Santos et al., 2013; Zhang et al., 2014) and their phytotoxic effects on seed germination and early seedling growth after being accumulated in soil by leaf leaching, plant residues decomposition and root exudation have been examined (Florentine and Fox, 2003; Ahmed et al., 2008; He et al., 2014). Leachate of Eucalyptus foliage, which contains a variety of oils and resins, exerts an direct/indirect allelopathic effect on neighboring species (e.g. plant roots and seeds, or soil microbes), thus reducing the abundance and richness of understory species (Ziaebrahimi et al., 2007; Ruwanza et al., 2015). However, other researchers do not agree with this (Silva et al., 1995; Yirdaw and Luukkanen, 2003; Zhang et al., 2016). They argued that supporting evidence for inhibitory effects of Eucalyptus were derived mainly from indoor experiments which focused on germination and root growth of sensitive weeds and crops (El-Khawas and Shehata, 2005; Carvalho et al., 2015), and there are few studies concerning the allelopathic effects of Eucalyptus on tree species in the field. Indeed, Eucalyptus can have a “catalytic effect” or “nurse effect” on the regeneration of natural forest biodiversity in degraded lands (Loumeto and Huttel, 1997; Feyera et al., 2002). On the other hand, a variety of factors, including environmental conditions (Yirdaw and Luukkanen, 2003), concentration of allelochemicals (Inderjit and Duke, 2003), and soil substrate (Parepa and Bossdorf, 2016) contribute to the variation in allelopathy. More field-based studies are needed to evaluate allelopathy under natural conditions. Increasing species diversity could enable a plant community to use a site’s resources more effectively (Petchey and Gaston, 2002; Kelty, 2006; Forrester et al., 2010; Li et al., 2014). Considering to the sustainable development of artificial forest, Chinese government is considering ways to reconstruct Eucalyptus plantation monocultures in an effort to reduce their possible negative ecological effects (Sun et al., 2017). Mixed plantations of Eucalyptus and native species have been proposed to maximize productivity and enhance ecological services of forest plantations (Turnbull, 1999; Forrester et al., 2005; Erskine et al., 2006; Wu et al., 2015). Many studies have reported that allelopathy is species-specific (Fang et al., 2009; Kim and Lee, 2011; Meiners et al., 2012) and the selection of species for reconstruction of Eucalyptus monocultures remains an issue (Tesfaye et al., 2015; Sun et al., 2017). In order to improve forest management, allelopathy and resource competition should be taken into consideration during species selection. The substrate (e.g. soil nutrients) can influence the production of allelochemicals by the donor species (Einhellig, 1996), and allelochemicals can interfere with nutrient acquisition in the target plant by negatively influencing mycorrhizal symbiosis (Stinson et al., 2006). Resource competition and allelopathy may operate simultaneously and/or sequentially, influencing community structure and vegetation dynamics (Inderjit and del Moral, 1997), but the exact nature and mechanisms of the interactions are poorly understood. In this study, we investigated the allelopathy and resource competition on woody species in E. urophylla plantations. First, we conducted a bioassay to test allelopathic effects of leaf aqueous extract of E. urophylla on root, stem growth and seed germination of twenty broadleaves woody species. Based on their sensitivities to the aqueous extracts, they were divided into two types (i.e. inhibited or uninhibited). And then, to assess the relative importance of allelopathy and resource competition, we planted the two groups of saplings into the E. urophylla plantation separately and treated with three gradients of irrigationnutrients and determined the seedling survival and basal growth of those twenty species.

2.1. Site description Experiments were carried out at Shuilian Moutain Forest Park, Dongguan city, Guangdong province, China (113°42′ E, 22°58′ N). The climate of the region is subtropical monsoon and a rainy season from April to September. The mean annual temperature is 23.2 °C and mean annual precipitation is 1780 mm. The soils are latosol developed on granite with a pH of 3.8. Shuilian Mountain Forest Park has an extensive practice of E. urophylla plantations, which have been established in 1992 and protected from any artificial disturbance after initial establishment. E. urophylla trees dominate the canopy with about 15–20 m high and the density of 10 individuals/100 m2. The average basal diameter of the trees is about 22 cm. A few native tree species distribute sporadically in the plantations, such as Diospyros morrisiana, Rhus sylvestris, Sapium discolor, Aporosa chinensis and Adinandra millettii. The shrub species cover is about 60%. Moreover, vertical stratification of shrub and herbaceous plants is not obvious, and the understory is dominated by shrub species such as Psychotria rubra, Ilex asprella and Adina pilulifera and herbaceous species such as Scleria levia, Microstegium vagans and Neyraudia reynaudiana. 2.2. Plant species Initially, we collected fifty-six broad-leaved tree species for the glasshouse experiment (Table S1). We collected seeds of fity-four native species from late 2005 to early 2006 from Heishiding Nature Reserve and Dinghushan Nature Reserve; both reserves are located in Southern China within 200 km radius of the studied plantations. Two species (Leucaena leucocephala and Albizia lebbeck) were introduced nitrogen (N)-fixing species and they were selected to improve soil fertility (Chen et al., 1999; Forrester et al., 2006; Hoogmoed et al., 2014). Some species, such as Castanopsis fissa, Erythrophleum fordii; Michelia maclurei and C. burmanni, were used to reconstruct the E. urophylla plantation (Wang et al., 2002; Yi et al., 2004). Many other species like Liquidambar formosana (Hamamelidaceae), Delonix regia (Leguminosae) and C. camphora (Lauraceae) were used to establish public ecological forests or scenic forest (Wang et al., 2002; Huang et al., 2006). Schima superba and M. maclurei were confirmed to be excellent choices for establishment of firebreak forest (Xue et al., 2005). 2.3. Experimental design 2.3.1. Experiment 1: Assessing the sensitivities of native species to allelopathic effects of E. urophylla Previous studies have shown that leaf leaching is the main allelopathic pathways of Eucalyptus. E. urophylla leaves contain a higher diversity and higher quantities of phenolics and terpenoids than roots (Turk and Tawaha, 2003). To get closer to the natural conditions, we assessed allelopathy of E. urophylla with water as extraction solvent (Vyvyan, 2002; Lorenzo et al., 2013). Before testing, we cleaned the seeds and sterilized them by soaking in 0.5% KMnO4 solution for 20–30 min, then rinsed in tap water three times (Fang et al., 2009). To prepare aqueous extracts of E. urophylla, we collected the leaves on different individuals by an aleatory sampling from the E. urophylla plantation at Shuilian Moutain Forest Park in autumn 2005. We chose the intact and healthy leaves, and then cleaned and cut them into pieces (1–2 cm). The stock solution of foliar extracts was prepared by soaking 100 g (fresh weight) in 1000 mL of deionized water for 24 h in darkness, and then filtered to make a stock solution (1:1) (Malik, 2004; Fernandez et al., 2016). Diluted solutions (1:7 and 1:10) were prepared from the stock solution with water. Aqueous extracts were stored at 4 °C until used. The three filtrates (1:1, 1:7 and 1:10) were treated as the aqueous 388

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2.4. Data analysis

extract treatments, while the distilled water was used as the control. Thirty or fifty seeds of each target species, depending on seed size, were placed in glass petri dishes with two pieces of filter paper, then regularly soaked with different aqueous extracts during the experiment. Each treatment was replicated three times. Petri dishes with seeds were placed in a growth cabinet at 28 °C, with a 12 h light/dark cycle. At the end of the experiment, we measured the number of germinated seeds, taproot length and stem length of seedlings for each species. Initially, there were fifty-six species tested in this experiment (Table S1). Due to severe mildew of seeds, twenty-five species failed to complete the aqueous extract bioassay (Table S1), including M. maclurei. However, considering M. maclurei is a superior afforestation tree species in south China (Kang et al., 2006), we conducted another bioassay for it subsequently. We sowed the seeds of M. maclurei into soil which had been collected from outside the plantation and soaked with aqueous extracts of E. urophylla regularly. Meanwhile, for the sake of the sequent field experiment, we systematically assessed the quantity and quality of seedlings. And then we chose twenty species as target species for the bioassay and divided them into two types, based on their response to the aqueous extract of E. urophylla leaves. The inhibited type (A) included species that were significantly inhibited by aqueous extracts at any concentrations, including seed germination and root growth and stem growth. The uninhibited type (B) comprised species which were stimulated or unaffected by the leaf aqueous extract.

In the laboratory experiment, Z test method (Cox 1996) was used to compare the seed germination ratios between the leachate treatments and the control. The Z value was calculated as:

Z=

PT −PC (PT − PC )[200 − (PT − PC )] 2N

where PT and PC are the seed germination rates of the treated group and the control, respectively, and N is the number of seeds used for the germination test. In this study, N = 30 or N = 50. The differences of root and stem growth between the treatments and the control were conducted by t-test. The irrigation-nutrients treatments were conducted according to the experimental design between Feb. 2007 and Aug. 2008 but ceased after Aug. 2008 due to various reasons. So, we analyzed the data by two different periods, (i) from Feb. 2007 to Aug. 2008 (i.e. 18 months), which represented early growth of seedlings, and (ii) from Feb. 2007 to June 2016, which represented relatively long-term growth (i.e. 112 months). We conducted Pearson correlations to investigate the possible relationship between seedling survival rate and relative growth rate of species type A and type B, respectively. One-way ANOVA was used to evaluate the differences on seedling basal growth and survival between type A and type B under different irrigation-nutrients treatments (P < 0.05). We carried out ANOVA to determine the effects of species type and resource treatments and their interactions on seedling survival and basal growth of the twenty target species. All statistical analyses were conducted with the software SPSS 22 for Windows.

2.3.2. Experiment 2: Testing the effects of allelopathy and irrigationnutrient treatments on seedling growth and survival in E. urophylla plantations To explore the mechanisms responsible for the loss of plant diversity in E. urophylla plantations, we planted seedlings of the selected 20 woody species (Experiment 1) into the field to evaluate the effects of allelopathy and resource addition on seedling growth and survival. The E. urophylla plantation was established in 1992 on a hill in Shuilian Moutain Forest Park. We set up 6 parallel transects (15 × 85 m for each) along the contours of the hillside in Jan. 2007. Each transect included 6 plots (10 × 10 m for each). We randomly chose three of them and planted with species type A (10 species) respectively at a density of 1 seedling/m2 (i.e. 100 seedlings per plot). The other three plots were planted with 10 species belonged to type B, with the same planting method. Thus, there were 3600 seedlings in total in this experiment (2 types × 3 plots × 10 species × 10 seedlings/plot × 6 transects = 3600). We built up buffer zones of 5 m width between plots. Before planting, we cleared the vegetation understory in the plantation, with four or five E. urophylla left in each plot. After planting the seedlings, we watered them every 2 d. We checked the status of each seedling and replaced those wilted or dead during the first 30 d. Three fertilization and irrigation treatments were randomly applied on each plot: (i) control was without fertilization or irrigation (CK); (ii) “low” treatments which were watered every 30 d and fertilized with 2.2 kg compound fertilizer every 4 months, and (iii) “high” treatments watered every 10 d and fertilized with 2.2 kg compound fertilizer every 2 months. In each transect, three plots planted with species type A were applied with the CK, “low” and “high” resource treatments respectively, and the same treatments were applied to the three plots planted with species type B. The K2SO4 compound fertilizer used in our experiment was produced by Norsk Hydro A.S. Co. Ltd and belonged to type of 15–15–15, according to the ratio of N: P: K. We first measured the basal diameter of each seedling in February 2007. Then, we recorded the survival status of each seedling and remeasured the basal diameter of live seedlings every 3 months. The relative growth rate (RGR) was calculated on the basal diameter increase of each seedling individual per year (Lambers and Poorter, 1992). The latest survey was conducted in June 2016.

3. Results 3.1. Allelopathic effects of E. urophylla aqueous extracts The effects of the aqueous extracts were stimulatory, inhibitory and neutral, depending on the target species and the concentrations (Table 1). Under three aqueous extract concentrations, 9, 6 and 3 species were negatively affected by the aqueous extracts during root growth, stem growth and seed germination, respectively. Negative effects of the aqueous extract were more pronounced at the relatively higher concentration (1:1) while positive effects happened at lower concentrations (1:7 and 1:10) (Table 1). Our results also suggested that allelopathic effects of aqueous extract of Eucalyptus were species-specific (Table 1). For the root growth and stem growth, the aqueous extract (1:1 and 1:7) exerted inhibitory effects on P. lanceaefolium, but they were stimulatory to C. camphora. For H. cochinchinensis, root and stem growth were significantly stimulated by aqueous extracts at the two lower concentrations (1:7 and 1:10), while the aqueous extracts had no effect at 1:1 concentration. Five species including S. superba, C. hui, C. burmanni, H. dulcis and O. glaberrima were not affected by aqueous extract of E. urophylla. Root length was negatively affected mostly (7 out of 20 receptor species). In contrast, only 3 species, including P. benthamiana, P. lanceaefolium and C. concinna, were affected by aqueous extract during seed germination (Table 1). As a whole, the higher concentrations of extract had a less stimulatory effect on target species than the lower one. According to the sensitivities of twenty target species, we divided them into type A (inhibited) and type B (stimulated or unaffected) (Tables 1, S3). Type A species were more sensitive to aqueous extract of E. urophylla and suffered more inhibitory effects than type B. The stem growth of M. maclurei was stimulated by the aqueous extract (Table S2). 3.2. The effects of allelopathy and irrigation-nutrient treatments in E. urophylla plantations Seedlings of species type A, which suffered more inhibitory effects, 389

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species, L. leucocephala and A. lebbeck showed the lowest survival and relative growth rate (Figs. 3, 4). However, nutrient-irrigation did not significantly affect survival and growth (P > 0.05), except for some species (i.e. C. chinensis, A. acuminatissima, P. lanceaefolium, S. superba and O. glaberrima) under some certain conditions (Figs. 3, 4). The species type did not interact with the resource treatment on neither survival nor basal diameter growth of the seedlings (Table 2). Survival was significantly correlated with relative growth rate regardless of allelopathic type (Fig. 5), and the slop of plant type B was smaller than type A in the early growth (Fig. 5). Thus, compared with the nutrient and water competition, the allelopathic trait was more important for the survival and growth of seedling understory of E. urophylla.

Table 1 The allelopathic effects of aqueous extracts of E. urophylla leaves on root/stem growth and germination of target species. Type

A

B

Species

Root

Stem

Germination

1:1

1:7

1:10

1:1

1:7

1:10

1:1

1:7

1:10

PhBe CaCh ScOc AcAc CaFi IiTr PtLa CrCo LeLe AlLe

- ** N - ** -* -* - ** -* N N N

N N N N N N -* N N N

N N N -* N N N N -* N

-* N N -* N N -* N + ** N

N -* + ** N N N -* N +* -*

N N + N N N N N N N

- ** N N N N N -* -* N N

N N N N N N N N N N

N N N N N N N N N N

CiCa ScSu CyHu CiBu HeCo CyMy MaCh HoDu OrGl MiMa

+ N N N N + N N N

**

+ N N N + N N N N

N N N N N N N N N

N N N N N N N N N N

N N N N N N N N N

**

**

+ N N N + N + N N N

**

*

*

+ N N N + N N N N

**

**

+ N N N N N N N N

**

+ N N N + N N N N +

*

**

**

**

*

4. Discussion The impact of E. urophylla plantations on the functions and processes of native forest ecosystems has received much attention (Stone, 2009). One main concern is that Eucalyptus plantations could negatively impact the diversity of native plants (Gaertner et al., 2011), thereby leading to shifts in the structure and properties of ecosystems (Yang et al., 2012). Although the methods applied in this study had limitations, the results indicated that the allelopathic effects of E. urophylla are important factors which impede the colonization and survival of other tree species.

The twenty tested species as follow: Photinia benthamiana, PhBe; Castanopsis chinensis, CaCh; Schefflera octophylla, ScOc; Acmena acuminatissima, AcAc; Castanopsis fissa, CaFi; Ilex triflora, IiTr; Pterospermum lanceaefolium, PtLa; Cryptocarya concinna, CrCo; Leucaena leucocephala, LeLe; Albizia lebbeck, AlLe; Cinnamomum camphora, CiCa; Schima superba, ScSu; Cyclobalanopsis hui, CyHu; Cinnamomum burmanni, CiBu; Helicia cochinchinensis, HeCo; Cyclobalanopsis myrsinaefolia, CyMy; Machilus chinensis, MaCh; Hovenia dulcis, HoDu; Ormosia glaberrima, OrGl; Michelia maclurei, MiMa. A refers to the species inhibited and B refers the species uninhibited (including stimulated and unaffected) by aqueous extract of E. urophylla. The extract of 1:1 is the stock solution which prepared by soaking 100 g (fresh weight) in 1000 mL of deionized water for 24 h and the diluted extract of 1:7 and 1:10 were prepared from the stock solution with water. The results of the bioassay are as depicted in the Table 1: “-”, “+” and “N” represent the inhibitory, stimulatory and neutral effects of aqueous extract when compared to the control, respectively. ** P < 0.01. * P < 0.05.

4.1. Allelopathic effects of aqueous extract of Eucalyptus The inhibitory effects of allelochemicals in Eucalyptus have been reported extensively (Mohamadi and Rajaie, 2009; Zhang and Fu, 2009; Zhang et al., 2012). Phenolic acids and volatile oils are considered to be two main categories of allelochemicals in Eucalyptus plants (Sasikumar et al., 2001), which impose significant inhibitory effects on plant growth. Terpenes were identified as major compounds in Eucalyptus leaf samples in previous studies (Grbović et al., 2010; Sahin Basak and Candan, 2010), as they have been reported to inhibit germination and radical elongation of other species such as wheat (Zahed et al., 2010). Eucalyptol, in particular, can inhibit growth of plant root and shoots by causing cork-screw-shaped morphological distortions as well as stress to photosynthesis (Romagni et al., 2000). A variety of phenolic compounds were identified from Eucalyptus tissues, litter leachates and affected soils, which are detrimental to growth of other plant species (Singh and Singh, 2003; Khan et al., 2008) due to the interference of phenolic compounds in the phosphorylation pathway and inhibition of the Mg2+ and ATPase activities (Sasikumar et al., 2001). Moreover, allelopathic effects of Eucalyptus have been shown to be species-specific (Sasikumar et al., 2001; Fang et al., 2009; Meiners et al., 2012; Chu et al., 2014), and this specific mechanisms may act at the cellular or molecular level (Niakan and Saberi, 2009), or in physio-morphology (Bughio et al., 2013). Although allelopathy is typically thought of as a mechanism of inhibition (Inderjit et al., 2011), it is broadly defined as any chemical mediated interactions (e.g. negative or positive) among plants (Rice, 1984). Results in the present study suggest that aqueous extracts of E. urophylla leaves exert variable effects (e.g. stimulatory or inhibitory) on root and stem growth depending on the concentration and the target species. These findings are consistent with the work of Ahmed et al. (2008), Espinosa-García (2008) and Fang et al. (2009). Roots and stems of C. camphora were triggered by aqueous extract at all three tested concentrations, and increased root and stem growth of H. cochinchinensis and S. octophylla were also detected in diluted extracts, 1:7 and 1:10 (Table 1). Some researchers proposed that overcompensation, related in part with induction of plant defenses, is the most probable pathways for hormetic responses (Belz and Duke, 2014). Although there are no studies that have focused on the mechanisms underlying the stimulatory effects of E. urophylla allelochemicals, it is surmised that the species that showed increased root and stem length have the potential

Table 2 Results of an ANOVA test assessing the effects of plant type and resource treatment on survival rate and relative growth rate of seedling. Period

Feb. 2007 to Aug. 2008 Feb. 2007 to June 2016

Parameter

Survival rate Relative growth Survival rate Relative growth

F-values Species type

Resource treatment

Species type × Resource treatment

21.27** rate 2.88 9.38** rate 4.25*

0.88 8.57** 0.03 0.37

0.12 1.07 0.08 0.29

** P < 0.01. * P < 0.05.

had significantly lower survival rates than those of species type B, in both the first and second periods (Feb. 2007 to Aug. 2008, and Feb. 2007 to June 2016) (Table 2, Figs. 1, 2). Seedlings of species type B grew faster than those of species type A in the second but not the first term (Table 2, Fig. S2). Higher nutrient-irrigation led to faster seedling growth in the first but not the second term (Fig. 2). However, the resource treatment did not have significant impacts on seedling survival. Overall, type B had a higher survival rate and higher relative growth rate than type A, regardless of resource treatment (Figs. 1, 2). The sensitive N-fixing 390

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Fig. 1. The effects of species types on survival rate of target tree species under three different fertilization and irrigation treatments. (a) The early growth period, Feb. 2007–Aug. 2008; (b) the relative long-term growth period, Feb. 2007–June 2016. A refers to the species are inhibited by aqueous extract of E. urophylla, while B is for the species which are stimulated or unaffected. ** and * indicate the significant difference between A and B under the same treatment at P < 0.01 and P < 0.05, respectively.

Fig. 2. The effects of species type on relative growth rate of target tree species under three different fertilization and irrigation treatments. (a) The early growth period, Feb. 2007–Aug. 2008; (b) the relative long-term growth period, Feb. 2007–June 2016. A refers to the species are inhibited by aqueous extract of E. urophylla, while B is for the species which are stimulated or unaffected. * indicates the significant difference between A and B under the same treatment at P < 0.05.

4.2. The relative importance of allelopathy and resource competition in E. urophylla plantations

to develop physiological defense mechanisms which allow them to escape specific types of chemical stress. Compared to root and stem growth, seed germination of tree species suffered from the least inhibitory effect of extract of E. urophyllla leaves (Table 1). It has been confirmed that α-amylase activity is a crucial factor for germination of some species by regulating starch breakdown (Mohamadi and Rajaie, 2009). Leaf leachates of E. globulus were reported to decrease α-amylase activity in seeds of finger millet (Eleusine coracanta). Many studies have illustrated that the allelopathic effects of Eucalyptus on seed germination of small and sensitive weed/crop species (Niakan and Saberi, 2009; He et al., 2014; Carvalho et al., 2015), but rarely focused on tree species (Del Fabbro et al., 2014). In this study, there were only three species where seed germination was inhibited by 1:1 aqueous extract of E. urophylla, and they were of smaller seed size than others species as we surveyed. Allelopathic effect is dosedependent (Reigosa et al., 1999; Sinkkonen 2006; Zhang et al., 2011). Allelochemicals must be taken up by the target plants in order to have a direct effect (Willis, 1985). However, the physical contact of the roots with phenolic acids is comparatively more important than the uptake (Blum et al., 1999). Thus, we speculate that large seed size and biomass will have an indirect dilution effect and the hard seed crust may effectively prevent the seed from absorption of allelochemicals.

As compared with the resource competition, the chemically-mediated interference on the distribution and abundance of plant species have been underestimated before. The results of this study indicate that plant type and resource availability are important factors that influence the plant biodiversity in Eucalyptus plantations. The allelopathic type, referring to sensitivity to aqueous extracts of E. urophylla, is a good predictor for seedling survival rate of target tree species, but also longterm seedling basal diameter growth. Additional fertilization and irrigation increased early growth of seedlings, but this advantage disappeared over time. Therefore, compared to resource competition, allelopathy is considered to be a more important factor affecting seedling growth and survival in the field (Table 2). Interestingly, we found that the growth of target tree seedlings was positively correlated with their survival (Fig. 5), and there was no evident trade-off between growth and chemical defense under allelopathic stress. Offense is the best defense. Allelopathic compounds can directly influence other species by decreasing their germination or growth (Prati and Bossdorf, 2004) or indirectly by disrupting mutualisms or stimulating soil-borne pathogens (Stinson et al., 2006; Mangla and Callaway 2008). The allelopathic effect is concentration-dependent, so the higher growth rate may contribute to the dilution of the concentration of putative allelochemicals by larger biomass. On the other hand, the higher growth rate of plant 391

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is generally an asymmetric competition, which larger individuals obtain a disproportionate advantages over smaller individuals (Freckleton and Watkinson, 2001). It will be vital in a long period with the plants grow up. Although we had cleared all vegetations understory of E. urophylla before we planted the seedlings into the plantation, the potential competition for light from canopy of E. urophylla on seedling survival and growth was not taken into account in this study. Second, the allelopathic effect is species-specific, but there were only twenty species involved in this study. More species should be planted inside and outside the E. urophylla plantations, which will make the comparisons between the inhibited and uninhibited species more convincing. 4.3. Implications for reconstruction of Eucalyptus plantations Establishment of mixed plantations is believed to be a sound silvicultural practice in tropical ecosystems in order to counterbalance the negative influence of Eucalyptus on soil nutrients and plant biodiversity (Bristow et al., 2006; Nouvellon et al., 2012; Santos et al., 2016). Many studies have focused on mixed plantations of N-fixing species and exotic tree species (Duarte et al., 2006; Forrester et al., 2006; Gareca et al., 2007), but mixed-species plantations that include E. urophylla have not been studied. Previous studies have reported that N-fixing species suffered less from the detrimental effect of Eucalyptus leachates (Chu et al., 2014) and can be used to alleviate adverse ecological effects of Eucalyptus monoculture (Bouillet et al., 2013; Forrester et al., 2013). In contrast, the three N-fixing species in our present study did not show better survival and growth than non-N-fixing species in the planting experiment. Also, A. lebbeck and L. leucocephala suffered the lowest survival rate and growth rate (Figs. 3, 4). Although the native N-fixing species, O. glaberrima, showed better survival and growth, we still cannot conclude that whether the divergence result from the origin of them (native versus non-native). Vegetation removal is often used as a common forest management practice seeking to conserve and restore native habitat types (Fork et al., 2015). Recent studies have shown that some exotic plants have the potential to leave an allelopathic “legacy effect” in the soils even after they have been removed (Siemens and Blossey, 2007) and continue to hinder the reintroduction of native plant species (Ruwanza et al., 2015). Transferring soil from uncolonized sites seems to be an effective option for eliminating the effects of allelochemicals to facilitate restoration. However, a great deal of cost is involved with this option, making it unrealistic in most cases. Eucalyptus plantations are used to meet the growing demand for timber products, and they can be used as pioneer species to sustain ecosystem functioning for degraded lands, and they are an important carbon sink (Wu et al., 2014; Wu et al., 2015). Some studies have shown that Eucalyptus can be used as nurse plants to improve seedling growth and plant biodiversity (Feyera et al., 2002; Lüttge et al., 2003). In the present study, the higher growth rate of saplings is associated with higher survival rate (Fig. 5), thus we suggest that the growth rate of native species is a critical reference for screening tree species in mixed Eucalyptus plantations. Although root and stem growth were triggered by the aqueous extract, C. camphora suffered low survival and growth rate in the relative long-term. However, H. cochinchinensis, which is a non-mycorrhizal species and belongs to Proteaceae, was stimulated by aqueous extract of E. urophylla; moreover, H. cochinchinensis also performed well in the field, with a relatively high survival and growth rate. Grevillea robusta which belongs to Proteaceae, is widely cultivated as a multiple-use agroforestry tree in many tropical countries (McGillivray and Makinson, 1993). Taking survival and growth into account systemtically, H. cochinchinensis, P. lanceaefolium, C. burmanni, M. chinensis, A. acuminatissima and C. chinensis would be good choices to intercrop with E. urophylla (Fig. S1). In addition, further research on the potential allelopathy of Eucalyptus should involve more tree species in order to promote understanding of the overall potential impact on native plant diversity, and to screen suitable species for reconstruction.

Fig. 3. The survival rate of 20 species under different fertilization and irrigation treatments in the early growth period from Feb. 2007 to Aug. 2008 (a) and in the relative long-term growth period from Feb. 2007 to June 2016 (b). The three irrigation-nutrient gradients are as follow: (i) Control, no watering, no fertilizing); (ii) Low, watered once if sunny for 30 days, fertilized every 4 months; (iii) High, watered once if sunny for 10 days, fertilized every 2 months. Values are the means ± SE of three treatments. Bars with asterisks are significantly different based on ANOVA and * indicates the significant difference with the control at P < 0.05. The correspondence between abbreviations and species names are given in Table 1.

Fig. 4. The relative growth rate of 20 species based on basal diameter under different fertilization and irrigation treatments in the early growth period from Feb. 2007 to Aug. 2008 (a) and in the relative long-term growth period from Feb. 2007 to June 2016 (b). The three irrigation-nutrient gradients are as follow: (i) Control, no watering, no fertilizing); (ii) Low, watered once if sunny for 30 days, fertilized every 4 months; (iii) High, watered once if sunny for 10 days, fertilized every 2 months. Values are the means ± SE of three treatments. Bars with asterisks are significantly different based on ANOVA and * indicates the significant difference with the control at P < 0.05. The correspondence between abbreviations and species names are given in Table 1.

will increase their competitiveness for resources and enhance the effects on culturing its species-specific microbial communities which benefit itself. Our study represents an field-based evidence that chemicallymediated interference is able to be a driving force for plant diversity in plantations and natural ecosystems (Fernandez et al., 2013; Scognamiglio et al., 2013; Del Fabbro and Prati 2015). However, there are several limitations for our study. First, species-specific growth and survival responses to resource competition (e.g. light) play a key role in determining forest composition (Hoste et al., 2011; Offord et al., 2014), especially in closed forests (Nicotra et al., 1999). Competition for light 392

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Fig. 5. The relationship between the relative growth rate and survival rate of two types of plants. (a) The early growth period, Feb. 2007–Aug. 2008; (b) the relative long-term growth period, Feb. 2007–June 2016. A refers to the species are inhibited by aqueous extract of E. urophylla, while B is for the species which are stimulated or unaffected. †† and ** indicate P < 0.01, which belonged to plants of type A and plants of type B, respectively.

In conclusion, our study shows that the effects of aqueous extract of E. urophylla leaves on tree species are species-specific, which may be stimulatory, neutral or inhibitory. Resource treatment has limited impacts on sapling establishment. The results suggest allelopathy is more important than resource competition in reducing native species biodiversity in E. urophylla plantations. The successful establishment of native woody communities will benefit from mixing species that are not inhibited by E. urophylla. We propose that H. cochinchinensis, P. lanceaefolium, C. burmanni, M. chinensis, A. acuminatissima and C. chinensis are good candidates for the reconstruction of E. urophylla plantations.

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