Facilitation by two exotic Acacia: Acacia auriculiformis and Acacia mangium as nurse plants in South China

Forest Ecology and Management 257 (2009) 1786–1793

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Facilitation by two exotic Acacia: Acacia auriculiformis and Acacia mangium as nurse plants in South China Long Yang a,b, Nan Liu a, Hai Ren a,*, Jun Wang a,b a b

Heshan National Field Research Station of Forest Ecosystem, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou 510650, China Graduate University of the Chinese Academy of Sciences, Beijing 100049, China

A R T I C L E I N F O

A B S T R A C T

Article history: Received 4 December 2008 Received in revised form 24 January 2009 Accepted 26 January 2009

Because of their high growth rate and tolerance to bare soil, two exotic Acacia species, Acacia auriculiformis and Acacia mangium, have been commonly planted in degraded areas of South China. With their large canopies and ability to fix nitrogen, the two Acacia species have also been considered to act as nurse plants for understory plants. The current study clarified the nursing effects of the Acacia species by comparing microclimate characteristics and physiological traits of native plant seedlings at three sites: under the canopies of the each Acacia species and on bare land (open site). Although the sites were not replicated, the results indicated that adult trees of both Acacia species can facilitate native species, but that A. mangium has greater facilitating effects due to greater temperature buffering, radiation reduction, and nutrient amelioration. In response to facilitation, three species (Castanopsis hystrix, Michelia macclurei, and Manglietia glauca) with different shade-tolerant traits growing under Acacia canopies expressed distinct adaptations. For the three species, the chlorophyll fluorescence curves of rETR and DF/ Fm0 were higher under A. auriculiformis and on the open site than under A. mangium. The maximum quantum yield in PSII(Fv/Fm) in diurnal changes of the three species showed that all the Fv/Fm values were between 0.70 and 0.84 and that the Fv/Fm values were mostly higher under A. mangium than on the open site or under A. auriculiformis. Total chlorophyll content and both chlorophyll a and b contents in the three species were higher under the Acacia species than on the open site, while chlorophyll a/b ratio was higher on the open site. In contrast, the carotenoid content in C. hystrix and M. macclurei was lower under the two Acacia species than on the open site, while the opposite was true for M. glauca. The results demonstrate that the adaptation of the understory species to abiotic environmental factors is not restricted to a single mechanism but apparently involves a group of interrelated, adaptive suites. And also these adaptations were species-specific and especially related to their shade tolerance. ß 2009 Elsevier B.V. All rights reserved.

Keywords: Nurse plants Facilitation Acacia auriculiformis Acacia mangium Exotic Acacia species South China

1. Introduction During the past several decades, forest degradation in China has accelerated, and the area affected by soil erosion has increased to 3.56  106 km2, representing about 37% of the country’s land area (SEPA, 2006). Among the degraded ecosystems, 3.74  106 ha are of degraded hilly slope-lands in South China (Zhang, 1994). In these tropical and subtropical degraded ecosystems, exotic fastgrowing species have been commonly used as pioneer plants to facilitate ecological restoration during the 20th century (Ren et al., 2007b). In addition to providing short-term protection of devastated soils and environments, the exotic species can also benefit the ecosystem by acting as nurse plants (Ewel and Francis,

* Corresponding author at: Xingke Road 723, Tianhe District, Guangzhou 510650, China. Tel.: +86 20 37252916; fax: +86 20 37252916. E-mail address: [email protected] (H. Ren). 0378-1127/$ – see front matter ß 2009 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2009.01.033

2004), although the latter phenomenon has not been studied in South China (Ren et al., 2008). Nurse plants are those that facilitate the growth and development of other plant species (target species) beneath their canopies by creating favorable microhabitats for seed germination and/or seedling recruitment (Franco and Nobel, 1989). There are also many other uses for nurse plants such as accelerating growth rates and nutrient cycling (Franco and Nobel, 1989; Callaway et al., 1991; Mazzarino et al., 1991), increasing light use efficiency (Gomez-Aparicio et al., 2006; Ishii et al., 2006), improving tree form and self-pruning (Troup and Johnston, 1956; Medhurst et al., 2003). The nursing effect may result from many factors including crown architecture, shading increment, temperature buffering, increases in soil moisture and nutrition, protection against herbivores, and enhancement of beneficial soil organisms (Padilla and Pugnaire, 2006; Callaway, 2007). The biology and usefulness of nurse plants have been investigated in many degraded habitats, including Mediterranean mountains,

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alpine habitats, arid deserts, semi-arid shrublands, savannas, ecotones between farmland and pasture, tropical sub-humid forests, and marshes (Bertness and Yeh, 1994; Callaway et al., 1996; Carrillo-Garcia et al., 1999; Castro et al., 2002; Arroyo et al., 2003; Sanchez-Velasquez et al., 2004; Armas and Pugnaire, 2005; Aerts et al., 2006). Recently, we began investigating the ecology of nurse plants in South China (Ren et al., 2008). Nurse plants play an important role in restoring the characteristics and functions of primary ecosystem. Facilitation, which in this case refers to the positive effect of certain plants on the establishment or growth of other plants, has long been recognized as a force that drives succession, especially in disturbed environment (Connel and Slatyer, 1977; Bruno et al., 2003). Besides native species, more attention was paid to exotic species as nurse plants in recent years in ecosystem restoration (Ewel and Francis, 2004; Jennings et al., 2003). Among the commonly planted exotics in South China, various fast-growing tropical pines, eucalyptus, and Acacia species are often used as pioneer trees so as to produce large amounts of raw wood and processed materials for industries. Because forest managers assumed that Eucalyptus spp. have allelopathic effects on native species (resulting in less seed germination and seedling recruitment, and even lower biodiversity), Acacia species, which have high growth rates, tolerance to poor soil, and substantial nitrogen-fixation ability, have been widely used for afforestation and greening in China and other countries (Peng et al., 2005; Nichols and Carpenter, 2006). Acacia, especially Acacia auriculiformis and Acacia mangium, were introduced to degraded tropical and subtropical regions to establish forest communities (Norisada et al., 2005; Peng et al., 2005; McNamara et al., 2006). These trees could not only improve soil nutrients, but by shielding against intense radiation and heat loading, they could also facilitate colonization by other plants (Parrotta et al., 1997; Lugo, 2004). Therefore, adult Acacia trees are considered as nurse plants for understory native species. The nursing effect of Acacia species, however, has not been adequately studied. Similarly, the physiological responses of some target species, including various climax tree species planted under these nurse trees, have not been studied in depth. The objectives of this study were (1) to clarify and compare the nursing effects of two Acacia species, A. auriculiformis and A. mangium and (2) to compare the responses of three shade-tolerant indigenous target species to the Acacia species; differences in the photosynthetic characteristics of the target species were quantified. 2. Materials and methods

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2.2. Tree species and experimental design A. auriculiformis and A. mangium are native to Australia and Indonesia (Norisada et al., 2005; Peng et al., 2005). They were introduced to China from Southeast Asia in 1961 and 1979, respectively, by the South China Botanical Garden, Chinese Academy of Sciences, and have been widely planted since the late 1970s because of their tolerance to harsh environments and especially of acid soils (Cole et al., 1996). The two Acacia species were used not only as urban trees but also as afforestation trees to conserve water and soil and to improve soil fertility in the hilly and coastal areas of Hainan, Guangdong, Guangxi, and Fujian Provinces (Peng, 2003). The three target species are all native to Southern China areas and are climax evergreen tree species; Castanopsis hystrix belongs to the family Fagaceae while Michelia macclurei and Manglietia glauca are members of the Magnoliaceae. They grow rapidly, have straight trunks, and grow better under Acacia canopies than in other habitats in South China (unpublished observation). C. hystrix can tolerate high moisture but cannot tolerate drought or low temperatures; it grows best in acidic red soil, yellow soil, and brick-red soil developed from granite and sandstone. Michelia macclurei is a mesophyte that prefers light and acidic soil; this species germinates quickly, has rapidly growing seedlings, and can tolerate dry and low-nutrient soil. M. glauca tolerates acidic soil and grows rapidly. These three native species are typical reforestation plants in South China. Each Acacia species was planted in one 1-ha site (one Acacia species per site such that each site was an ‘‘Acacia site’’). The spacing between trees was 3 m  3 m. The pure sites of A. auriculiformis or A. mangium, had an average height of 18 m and the trees were 15 years in 1998; in that year, 1-year-old seedlings (about 20 cm tall) of three native target species (C. hystrix, M. macclurei, and M. glauca) were randomly transplanted under the Acacia canopies or on an open site with similar area (c. 1 ha) and topography about 200 m from the pure plantations. The aspects of the three sites were all southeast-faced slope, and neighbouring buffering vegetation were shrub species R. tomentosa, and ferny D. dichotoma. The native target seedlings were watered and fertilized when transplanted and then grew naturally. They were 4–5 m high with 3–5 cm diameter at breast height in 2007, when the current study was conducted. Within each of the three unreplicated sites, 15 plots (1.5 m  1.5 m) were randomly selected and designed in between Acacia trees. Each plot contained only one healthy target species, and plots were separated by at least 1.5 m. In summary, the study included 3 sites (A. auriculiformis, A. mangium, and an open site) and 15 plots per site (5 plots for each of the 3 target native species). There were 45 plots in total.

2.1. Study area 2.3. Canopy characteristics and microenvironment The Heshan National Field Research Station of Forest Ecosystem (228400 N, 1128500 E), one of the core stations of the Chinese Ecological Research Network, has a total area of about 170 ha. The mean annual temperature at the station is 21.7 8C, and the mean annual radiation is 435.47 kJ cm2. The annual rainfall is about 1801.8 mm and annual evaporation is 1600 mm. On the red soil, the climax vegetation is low subtropical monsoon evergreen broadleaved forest. As a result of long-term serious disturbances, however, the soil has eroded and the original vegetation has almost disappeared (Yu and Peng, 1996). Therefore, ecosystem restoration has been carried out since 1983, and A. auriculiformis or A. mangium were planted as experimental plantations in the communities in the early stage of succession. Shrub and grass species (such as Rhodomyrtus tomentosa, Ilex asprella, Eurya chinensis, Clerodendron fortuneatum, and Dicranopteris dichotoma) have naturally grown under the Acacia canopies.

Community leaf area indices (LAIc) for the Acacia species were recorded in June 2007 with a LAI-2000 Plant Canopy Analyzer (LICOR, Inc., USA) for each Acacia site. Measurements were taken with a LAI-2050 optical probe (LAI-2000 Plant Canopy Analyzer accessory) on cloudy days. The LAIc and standard errors were calculated by the LAI 2000 data-logger. Data of air temperature (TA), relative air humidity (RHA), and soil temperature (0, 5, 10, 15, and 20 cm deep; TS) in 2007 in the A. auriculiformis, A. mangium, and open site were taken from Heshan National Field Research Station of Forest Ecosystem. Microenvironmental data from eight continuous clear days in July (the hottest month) and February (the coldest month) were selected for analysis. For determination of chemical characteristics, each soil sample consisting 5 soil cores was 5 cm diameter and 20 cm deep per plot.

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The cores were collected after the surface litter was removed. Each sample was mixed and air-dried in the laboratory. The soil samples were passed through a 2-mm sieve and analyzed for pH, soil organic matter (SOM), total soil nitrogen (TN), total soil phosphorus (TP), hydrolyzed nitrogen (HN), available phosphorous (AP), and soil exchangeable Na, K, Ca, and Mg. For determination of physical characteristics, nine intact soil cores were taken randomly in each site using ring knifes after the litter and humus layer had been removed. Three cores were used to determine soil bulk density (SBD), soil moisture content at saturation (SSM), and soil capillary moisture (SCM) in each plot. For determination of SSM, intact soil cores were laid on saturated filter paper until saturated; the weights of the saturated soil and dry soil were determined. For determination of SCM, the soil cores were placed in salvers to absorb water through capillary action via filter paper until the weight stabilized, usually after 8 h; the weights of the moist soil and dry soil were determined. Both SSM and SCM were expressed as percentage moisture as g of water per 1 g of dry soil. Soil bulk density (g of dry soil/cm3 of soil) was determined by weighing the intact soil cores after oven-drying at 105 8C. Both soil chemical and physical characteristics were analyzed with standard methods at the South China Botanical Garden and the Guangdong Institute of Eco-Environment and Soil Sciences (Liu, 1996; Duan et al., 2008). 2.4. Measurement of growth We used basal diameter to represent the growth of three target species. The basal diameter of one individual of the three target species was measured with diameter tape per plot in September 2008. 2.5. Chlorophyll fluorescence Chlorophyll fluorescence indices in the three target species were measured with a portable pulse-amplitude modulated chlorophyll fluorometer (PAM-2100, Heinz Walz, Effeltrich, Germany). Fully expanded leaves at the top of the crown of each target plant were sampled. The diurnal changes of maximum quantum yield of photosystem II (Fv/Fm) were measured on plant leaves (five leaves per individual) after 30 min of dark adaptation with dark leaf clips (DLC-8, PAM-2100 fluorometer accessory) at 2.5-h intervals on sunny days. The Fv/Fm values were calculated as Fv/Fm = (Fm  F0)/ Fm, where F0 is the minimum fluorescence, Fv is the maximum variable fluorescence, and the Fm is the maximum fluorescence. Chlorophyll fluorescence rapid light curves (RLCs) were measured by recording the chlorophyll fluorescence parameters, including electron transport rate (rETR) and actual photochemical efficiency of PS II in the light (DF/Fm0 ), with a standard 2030-B leaf clip holder (PAM-2100 fluorometer accessory). To generate RLCs, leaves were irradiated with a series of actinic light intensities (97, 157, 238, 358, 536, 737, 1010, 1551 and 2431 mmol m2 s1) for 10 s, always finishing with a saturating pulse after each level of illumination. DF/ Fm0 was calculated as DF/Fm0 = 1  Fs/Fm0 , where Fs is steady state fluorescence yield and Fm0 is the maximum fluorescence yield after light adaptation. The relative electron transport rate (rETR) can gain from 0.84  0.5  DF/Fm0  PAR, where 0.84 was the coefficient of absorption of the leaves, 0.5 was the fraction of electrons involved in the photoexcitation produced by on quantum, as two photosystems are involved, and PAR was the actinic photosynthetically active radiation generated by the internal halogen lamp of PAM-2100.

of the extracted solutions was measured using an ultraviolet (UV)– visible spectrophotometer (UV-2802, Unico, Shanghai). Total Chl, Chl a, Chl b and carotenoid contents were calculated based on leaf areas according to Lin et al. (1984). 2.7. Statistical analysis Data are presented as means  standard deviations (S.D.s). Oneway ANOVA were used to compare the effect of site (A. auriculiformis, A. mangium, or the open site) on microclimate data and physical and chemical characteristics of the soil. Least significant difference (LSD) tests were used for post hoc multiple comparison. Chlorophyll content of the shade-tolerant species was analyzed by a two-way ANOVA (three species  three types of sites), and the differences between species and site type were compared with LSD tests. All statistical analyses were done with SPSS 13.0 (SPSS Software Inc., USA). 3. Results 3.1. Canopy characteristics and microenvironment at Acacia sites The canopy leaf areas index (LAIc) in summer was significantly larger for A. mangium (2.71  0.10) than for A. auriculiformis (1.09  0.03). On the hottest days, the abiotic microenvironment, except for RHA (p = 0.386), significantly differed (p < 0.001) between sites with Acacia species vs. the open site (OS), but abiotic variables did not differ between sites with A. auriculiformis and A. mangium (p > 0.05) (Table 1). On the coldest days, air temperature and soil temperature (5 cm deep) differed significantly among the three sites (p = 0.002 and 0.040, respectively), but the other abiotic variables did not differ among the three kinds of sites. In addition, the abiotic variables did not differ between A. auriculiformis and A. mangium, except that the soil temperature 5 cm and 15 cm deep was greater in the A. mangium site than in A. auriculiformis site (Table 1). Soil physical characteristics, including SBD, SSM, and SCM, were all significantly different among the three sites (p = 0.024, 0.000, and 0.001, respectively) (Table 2). The A. mangium site had the highest SSM and SCM values and the lowest SBD value. In contrast, the open site had the lowest SSM and SCM values but the highest SBD value. Most soil chemical characteristics differed among the sites but pH and available phosphorous (AP) did not differ among the sites (p = 0.144 and 0.555, respectively) (Table 2). SOM, HN, and TP differed among the three sites (p = 0.008, 0.034, and 0.005, respectively), and the values were highest in the A. mangium site and lowest in the open site. TN was greater in the A. mangium site than in the open site (p = 0.044), although TN did not differ among the three sites (p = 0.103). Exchangeable K, Ca, and Mg did not differ among the three sites (p = 0.696, 0.094 and 0.377, respectively), but Na content was greater (p = 0.045) in the A. mangium site than in the open site. 3.2. Basal diameter in the three target species Similar results showed in all the three species that the basal diameters in the A. mangium site were higher than those in the A. auriculiformis site and on open site (Fig. 1). The basal diameters of C. hystrix and M. macclurei in A. auriculiformis site were higher than those on open site, while no statistical differences were found in M. glauca.

2.6. Total Chl and carotenoid contents

3.3. Rapid light curves of chlorophyll fluorescence in the three target species

The target species were sampled by removing 10 leaf disks (3 cm radius) from each of five plants per species in each plot. The leaf disks were extracted with 80% acetone for 5 days. Absorption

With the increase of actinic light, relative electron transport rate of PS II (rETR) of all three target species was elevated, while the actual photochemical efficiency of PS II (DF/Fm0 ) decreased. The

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Table 1 Abiotic variables in three kinds of sites (A. auriculiformis, A. mangium, and open site) on the hottest days (from July 28 to August 4 in 2007) and coldest days (from February 1 to February 8 in 2008). Abiotic variables

Season

AA

AM

OS

TA (8C)

Summer Winter

28.74  0.46 a 6.16  0.90 a

28.54  0.33 a 6.61  0.56 a

30.69  1.61 b 7.66  0.71 b

F 11.575 8.788

<0.001 0.002

p

RHA (%)

Summer Winter

0.52  0.12 a 0.56  0.11 a

0.50  0.16 a 0.61  0.17 a

0.43  0.12 a 0.48  0.18 a

0.996 0.997

0.386 0.394

TS 0 cm (8C)

Summer Winter

29.38  1.32 a 8.40  1.38 a

28.68  1.08 a 8.69  0.81 a

33.75  3.01 b 7.95  2.32 a

15.130 0.412

<0.001 0.668

TS 5 cm (8C)

Summer Winter

28.54  0.16 a 8.45  0.51 a

28.03  0.46 a 9.30  0.58 b

33.00  1.47 b 9.00  1.04 ab

74.922 2.611

<0.001 0.097

TS 10 cm (8C)

Summer Winter

28.04  0.26 a 8.90  0.46 a

27.64  0.36 a 9.45  0.49 a

31.83  0.96 b 9.07  0.64 a

114.685 2.193

<0.001 0.136

TS 15 cm (8C)

Summer Winter

28.26  0.17 a 9.26  0.52 a

27.63  0.32 a 9.88  0.38 b

31.75  0.57 b 9.70  0.50 ab

263.211 3.768

<0.001 0.040

TS 20 cm (8C)

Summer Winter

27.71  0.27 a 9.73  0.44 a

27.37  0.21 a 9.68  1.16 a

30.70  0.54 b 10.17  0.33 a

193.074 1.078

<0.001 0.358

Values are means  S.D. of eight replicates. Within each row, means with the same letter are not significantly different at p > 0.05. TA — air temperature, RHA — relative air humidity, TS — soil temperature, AA — A. auriculiformis, AM — A. mangium, OS — open site.

Table 2 Physical and chemical characteristics of soil in three sites (A. auriculiformis, A. mangium, and open site). Soil characteristics

AA

pH SOM (mg/kg) SBD (g/L) SSM (g of water/g of dry soil) SCM (g of water/g of dry soil) TN (%) HN (mg/kg) TP (%) AP (mg/kg) K (mg/kg) Ca (mg/kg) Na (mg/kg) Mg (mg/kg)

4.313  0.201 1.559  0.229 1.135  0.170 0.389  0.055 0.358  0.016 0.092  0.010 89.333  3.786 0.015  0.002 3.600  3.857 6.719  0.166 7.554  0.620 2.237  0.061 1.270  0.049

a a a b b ab ab a a a a ab a

AM

OS

F

p

4.127  0.072 a 2.113  0.136 b 1.013  0.104 a 0.484  0.024 c 0.380  0.049 b 0.103  0.026 b 105.667  16.921 b 0.024  0.003 b 4.667  4.726 a 7.512  0.814 a 7.709  2.237 a 2.448  0.260 b 1.410  0.271 a

4.650  0.433 a 1.284  0.252 a 1.387  0.067 b 0.218  0.008 a 0.213  0.008 a 0.067  0.011 a 71.667  10.599 a 0.015  0.011 a 1.367  1.436 a 8.592  4.467 a 4.975  0.712 a 1.961  0.167 a 1.932  0.935 a

2.718 11.930 7.448 44.544 27.609 3.394 6.301 14.955 0.650 0.385 3.597 5.407 1.152

0.144 0.008 0.024 0.000 0.001 0.103 0.034 0.005 0.555 0.696 0.094 0.045 0.377

Values are means  S.D. of three replicates. Within each row, means with the same letter are not significantly different at p > 0.05. AA = A. auriculiformis site, AM = A. mangium site, OS = open site. Note: SOM — soil organic matter, TN — total soil nitrogen, TP — total soil phosphorus, HN — hydrolyzed nitrogen, AP — available phosphorous, K — exchanged particle potassium, Ca — exchanged particle calcium, Na — exchanged particle sodium, Mg — exchanged particle magnesium, SBD — soil bulk density, SSM — soil moisture content at saturation, SCM — soil capillary moisture.

curves of rETR and DF/Fm0 were similar in the A. auriculiformis site and on the open site, but were lower in the A. mangium site than in the other two sites (Fig. 1). Also, the maximum rETR points in RLC of the three species were lower in the A. mangium site than in the A. auriculiformis site and on the open site (Fig. 1). 3.4. Diurnal changes of Fv/Fm in three target plants The diurnal changes of the maximum quantum yield in PS II (Fv/ Fm) are shown in Fig. 2. All the values of Fv/Fm in leaves of the three target plants were greater than 0.70 but less than 0.84. Fv/Fm values of the three species were usually higher in the A. mangium site. Fv/Fm values tended to remain relatively constant in the A. mangium site but tended to decline during the day on the open site and in the A auriculiformis site. The lowest diurnal values for all three species were measured on the open site; the lowest for M. macclurei, C. hystrix, M. glauca were at 14:30, 12:00, and 9:30, respectively. The values for all three species in the A. auriculiformis site dropped in the middle of the day (Fig. 3). Fig. 1. Basal diameters of three target species (Castanopsis hystrix, Michelia macclurei and Manglietia glauca) in three different sites in 2008. AA = A. auriculiformis site; AM = A. mangium site; and OS = open site. Values are means of five replicates. Bars with the same letter are not significantly different at p > 0.05.

3.5. Photosynthetic pigment content of three target plants The total chlorophyll (Chl T), chlorophyll a (Chl a), and chlorophyll b (Chl b) contents in C. hystrix leaves were highest

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Fig. 2. Electron transport rate-rapid light response curves of three target species (Michelia macclurei, Manglietia glauca, and Castanopsis hystrix) to a series of actinic light illuminations in three different sites. AA = A. auriculiformis site; AM = A. mangium site; and OS = open site. Values are means of three replicates.

Fig. 3. Diurnal changes of maximum photochemical efficiency of PS II (Fv/Fm) in three shade-tolerant plants (Michelia macclurei, Manglietia glauca, and Castanopsis hystrix) growing in three sites (A. auriculiformis, A. mangium, and open site). AA = A. auriculiformis site; AM = A. mangium site; and OS = open site. Each value is the mean  S.D. of three replicates.

Table 3 Photosynthetic pigment content for three shade-tolerant plants (C. hystrix, M. macclurei, and M. glauca) growing in three sites (AA = A. auriculiformis, AM = A. mangium, and OS = open site). Physiology indices

Sites

Target tree species C. hystrix

M. macclurei

M. glauca

Chl T

AA AM OS

2.06  0.31 b 2.93  0.20 b 1.91  0.28 b

3.64  0.23 a 3.29  0.13 a 2.47  0.16 a

4.23  0.54 a 3.20  0.22 ab 2.54  0.05 a

Chl a

AA AM OS

1.54  0.22 b 2.13  0.13 b 1.60  0.23 b

2.64  0.17 a 2.37  0.09 a 1.92  0.12 a

3.01  0.37 a 2.27  0.16 ab 1.91  0.04 a

Chl b

AA AM OS

0.52  0.08 c 0.80  0.07 b 0.32  0.06 b

1.00  0.06 b 0.92  0.05 a 0.56  0.05 a

1.23  0.17 a 0.93  0.06 a 0.63  0.02 a

Chl a/b

AA AM OS

2.96  0.06 a 2.66  0.09 a 5.11  0.61 a

2.65  0.03 b 2.57  0.05 a 3.44  0.12 b

2.46  0.07 c 2.44  0.01 b 3.03  0.04 b

Carotenoid

AA AM OS

0.40  0.06 b 0.48  0.03 b 0.59  0.07 b

0.72  0.03 a 0.65  0.01 a 0.73  0.01 a

0.72  0.09 a 0.70  0.05 a 0.67  0.10 ab

Values are means  S.D. of three replicates. Means in a row with the same letter are not different significantly at p > 0.05 for the target tree species.

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in the A. mangium site and lowest on the open site, while the opposite was true for carotenoid contents and Chl a/b ratios (Table 3). However, pigment combinations of the other two species (M. macclurei and M. glauca) responded differently to the three types of site. The contents of Chl T, Chl a, and Chl b in M. macclurei and M. glauca were higher in the A. auriculiformis site than in the A. mangium site or on the open site. Carotenoid and Chl a/b ratios for M. macclurei and M. glauca leaves were higher in the open site than in the A. auriculiformis or A. mangium sites. Chlorophyll content significantly differed among the three sites and the three target species, but carotenoid content did not significantly differ among the three sites. Chlorophyll content did not differ between A. auriculiformis and A. mangium sites but were greater in the Acacia sites that on the open site. 4. Discussion Acacia species, especially A. auriculiformis and A. mangium, have the strong potential to increase soil nutrition because their root nodules have the ability to fix nitrogen (Norisada et al., 2005; Peng et al., 2005). In the present study, total soil nitrogen and hydrolyzed nitrogen were higher under the two Acacia species than in the open site (Table 2) and higher under A. mangium than under A. auriculiformis. Ding et al. (1991) found that the quantities of nitrogen fixation by A. mangium were about 55.5–157 kg year1 per 1 ha land, which was obviously more than A. auriculiformis in the same place. It was different from these studies that nitrogen fixation was higher in A. auriculiformis than in A. mangium on poor sandy savanna soil in Congo (Bernhard-Reversat, 1996). In the highly weathered soils of tropical forests, organic matter is essential for soil function and forest sustainability (Macedo et al., 2008). After forests are removed, however, soil organic matter is lost to erosion and oxidation. According to our former studies (Ren et al., 2007a), nutrient cycling on these deforested sites recovered very slowly without artificial interference, i.e., artificial plantations are required to accelerate the restoration process. In the current study, in which the Acacia species had grown for more than 20 years, soil organic matter levels were significantly higher under A. mangium than under A. auriculiformis or on the open site. As was the case with nitrogen, soil organic matter increased more with A. mangium than with A. auriculiformis. Increased soil organic matter should benefit the shade-tolerant understory plants. Whereas both Acacia species increased soil N and organic matter, they did not affect the exchangeable cations K, Ca, and Mg, but A. mangium did increase soil Na concentrations. Light can influence plant physiology and metabolism through photosynthesis (Miyazawa et al., 2006; Kelly et al., 2009). Light could also be an important factor affecting forest formation and succession in South China (Peng and Wang, 1993). The canopies of both of the exotic Acacia species reduce solar radiation and thereby decrease the photoinhibition of understory species and also protect photosynthetic organs from strong light; with the reduction in solar radiation, the understory plants are able to assimilate more carbon and accumulate more biomass aboveand belowground (Valladares et al., 2005). Fv/Fm is an important measure of photochemical potential and stabilized between 0.80 and 0.85 (Bjo¨rkman and Demmig, 1987). When Fv/ Fm declines to less than 0.80, photoinhibition is likely appeared (Vonshak et al., 1994). In the current study, the three shadetolerant understory plants experienced obvious photoinhibition in the open site and under A. auriculiformis but not under A. mangium. However, the Fv/Fm values measured in the current study were always higher than 0.70, indicating that photosystem II did not suffer from high radiation stress, regardless of understory species or site type. Fv/Fm was higher and more

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constant under A. mangium than under A. auriculiformis, indicating that A. mangium provided better shading than A. auriculiformis. With respect to the long-term effects of shading, the three understory species are well suited to harvesting light in shade. Chl T was higher in plants growing under the two Acacia species than on the open site, indicating that the two Acacia species can facilitate the understory species. Chl a/b in the leaves was lower for plants growing under the Acacia species (2.44–2.96) than on the open site (3.03–5.11); Chl b exists mostly in the Chl a/b–protein complex (LHC) in both photosystems and improves light absorption to maintain the photosynthetic apparatus. In the present study, Chl b of C. hystrix on the open site decreased significantly, leading to an increase in Chl a/b. The understory species can also change pigment content to adapt to different light environments. The different proportions of chloroplast antenna pigment (mostly Chl b) and photosystem reaction centre pigment (mostly Chl a), which changed substantially with the different conditions under the Acacia species, indicated that the strongest nursing effect was experienced by C. hystrix. With respect to the short-term effects of shading, the canopy of A. mangium protects the understory species from intense light radiation and high-temperature stress at noon. Carotenoid content in leaves of similar ages indicated antioxidant activity and strong light-tolerance capability. Carotenoid content in C. hystrix and M. macclurei was lower under the two Acacia species than on the open site, indicating that the Acacia species can protect from photoinhibition through carotenoid increment. In addition, the LAIc was higher for A. mangium than for A. auriculiformis, because the leaf area is larger for A. mangium than for A. auriculiformis (Norisada et al., 2005; Peng et al., 2005), and therefore A. mangium produces a denser canopy and greater shading. Because the level of shading differed between the two Acacia species, the understory plants differed in shade-tolerance traits. The maximum rETR values in the three species were lower under A. mangium than under A. auriculiformis and on the open site, indicating that the understory species under A. mangium were deficient in their ability to respond to instantaneous increases in light intensity and that the leaves were shadetolerant. Also, the results showed that under A. mangium rather than under A. auriculiformis or on the open site, M. glauca had a higher relative electron transport rate and a higher actual photochemical efficiency of PS II in response to increasing light intensities but a lower variational range, indicating that M. glauca can adapt to shade. Thus, the light saturation points of rETR and DF/Fm0 in the three species were lower under A. mangium than under A. auriculiformis or on the open site, and the three species under A. mangium were not sensitive in response to instantaneous increasing light intensities, indicating that the leaves showed some shade-tolerance traits and that A. mangium had a better shading effect. Other factors provided by nurse plants can also improve the growth of the understory species. Air temperature and soil temperature were lower under A. auriculiformis and A. mangium than on the open site on the hottest days of the year, indicating that the two Acacia species can buffer the maximum temperature. Whereas air temperature and soil temperatures on the open site exceeded 30 8C, which is too hot for the understory plants, these temperatures were always less than 30 8C under the two Acacia species. On coldest days, however, soil temperature did not differ between the open site and under the two Acacia species, indicating that low temperature was not the reason for the nursing effect. The situation is different in higher latitudes and alpine areas, where temperature buffering is more important on the coldest rather than on the warmest days (Cavieres et al., 2006; Drezner, 2007). In southern Thailand, A. mangium could be nurse tree to dipterocarp

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species not for increment of nitrogen content of surface soil, but for providing moderate microclimate on severely degraded sandy soil (Norisada et al., 2005). Although atmospheric relative humidity was higher under the two Acacia species than on the open site, the difference was not significant, suggesting that increased atmosphere relative humidity was not an important factor in the nursing effect. 5. Conclusions In summary, the results of this study, although unreplicated for the effect of site, indicate that Acacia trees can act as nurse plants for understory species by increasing soil nitrogen and soil organic matter, by improving conditions for photosynthesis, and by buffering air and soil temperatures. The shading provided by the Acacia species, and especially by A. mangium, reduces the photosynthetic photoinhibition of the understory plants, which is beneficial to accumulate more biomass from carbon assimilation. The adaptation of the understory species to abiotic environmental factors is not restricted to a single mechanism but apparently involves a group of interrelated, adaptive suites (Shang, 2004). These adaptations were species-specific and especially related to shade tolerance. Acknowledgements This research was funded by National Natural Science Foundation of China (No. 40871249), the National Basic Research Program of China (2009CB421101) and International Foundation for Science (D/4539-1). The authors are indebted to Dr. Ping Zhao and Dr. Xi’an Cai for helpful comments, Prof Bruce Jaffee for suggestions and editing, Mr. Yongbiao Lin and Mr. Xingquan Rao for field assistance. We also thank anonymous reviewers for their valuable comments on the early version of the manuscript. References Aerts, R., November, E., Van Der Borght, I., Behailu, M., Hermy, M., Muys, B., 2006. Effects of pioneer shrubs on the recruitment of the fleshy-fruited tree Olea europaea ssp. cuspidata in Afromontane savanna. Applied Vegetation Science 9, 117–126. Armas, C., Pugnaire, F.I., 2005. Plant interactions govern population dynamics in a semi-arid plant community. Journal of Ecology 93, 978–989. Arroyo, M.T.K., Cavieres, L.A., Penaloza, A., Arroyo-Kalin, M.A., 2003. Positive associations between the cushion plant Azorella monantha (Apiaceae) and alpine plant species in the Chilean Patagonian Andes. Plant Ecology 169, 121–129. Bernhard-Reversat, F., 1996. Nitrogen cycling in tree plantations grown on a poor sandy savanna soil in Congo. Applied Soil Ecology 4, 161–172. Bertness, M.D., Yeh, S.M., 1994. Cooperative and competitive interactions in the recruitment of Marsh Elders. Ecology 75, 2416–2429. Bjo¨rkman, O., Demmig, B., 1987. Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77 K among vascular plants of diverse origin. Planta 170, 489–504. Bruno, J.F., Stachowicz, J.J., Bertness, M.D., 2003. Inclusion of facilitation into ecological theory. Trends in Ecology & Evolution 18, 119–125. Callaway, R.M., 2007. Positive Interactions and Interdependence in Plant Communities. Springer, Dordrecht. Callaway, R.M., DeLucia, E.H., Moore, D., Nowak, R., Schlesinger, W.H., 1996. Competition and facilitation: Contrasting effects of Artemisia tridentata on desert vs montane pines. Ecology 77, 2130–2141. Callaway, R.M., Nadkarni, N.M., Mahall, B.E., 1991. Facilitation and interference of Quercus douglasii on understory productivity in central California. Ecology 72, 1484–1499. Carrillo-Garcia, A., de la Luz, J.L.L., Bashan, Y., Bethlenfalvay, G.J., 1999. Nurse plants, mycorrhizae, and plant establishment in a disturbed area of the Sonoran Desert. Restoration Ecology 7, 321–335. Castro, J., Zamora, R., Hodar, J.A., Gomez, J.M., 2002. Use of shrubs as nurse plants: a new technique for reforestation in Mediterranean mountains. Restoration Ecology 10, 297–305. Cavieres, L.A., Badano, E.I., Sierra-Almeida, A., Gomez-Gonzalez, S., Molina-Montenegro, M.A., 2006. Positive interactions between alpine plant species and the nurse cushion plant Laretia acaulis do not increase with elevation in the Andes of central Chile. New Phytologist 169, 59–69.

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