The role of fire in the Central Yunnan Plateau ecosystem, southwestern China

Forest Ecology and Management xxx (2015) xxx–xxx

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The role of fire in the Central Yunnan Plateau ecosystem, southwestern China Wen-Hua Su ⇑, Zhan Shi, Rui Zhou ⇑, Yuan-Jiao Zhao, Guang-Fei Zhang Institute of Ecology and Geobotany, Yunnan University, Kunming 650091, China

a r t i c l e

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Article history: Received 23 November 2014 Received in revised form 10 May 2015 Accepted 11 May 2015 Available online xxxx Keywords: Evergreen broad-leaved forest Heat shock Post-fire regeneration Re-sprouting Serotiny Wildfire

a b s t r a c t Fire plays a major role in fire-dependent ecosystems in shaping plant traits, community assemblage, and in maintaining biodiversity and sustaining ecosystems. Excluding fire from fire-dependent ecosystems can substantially alter these ecosystems. This study mainly investigates the how the zonal vegetation evergreen broad-leaved forests as well as widely distributed vegetation Pinus yunnanensis forest and shrubland in the Central Yunnan Plateau adapt to fire, and addresses the role of fire in the Central Yunnan Plateau ecosystem to determine whether this ecosystem is fire-dependent. Re-sprouting trees and shrubs composed about 90.6% of the dominant taxa. In re-sprouting species, 41 species (77.4% of all re-sprouting species) were observed re-sprout from underground basal burls after a fire. After a fire, 100% of all trees and tall shrubs, 93.6% of all shrubs and 73.9% of all herbs recovered. Two serotinous tree taxa were found, including two varieties of P. yunnanensis (var. pygmaea and var. yunnanensis) which is a dominant and the most common tree species in this region. All these were identified here as weakly serotinous species. The degree of serotiny was 50.4% for P. yunnanensis var. yunnanensis and 74.7% for var. pygmaea. Heat shock resulted in higher seed germination rates for both varieties of P. yunnanensis. Dominant and common taxa in these two typical forest types had typical traits of species known to be adapted to fire; forest fire did not significantly reduce number of species. Based on the above results, the Central Yunnan Plateau ecosystem is a fire-dependent system. Wildfire plays an important role in the community assembly for the semi-humid evergreen broad-leaved forests, P. yunnanensis forest and shrub communities. Wildfire should not be viewed as a totally catastrophic event in forests of the Central Yunnan Plateau. In theory this region appropriates to carry out prescribed burning. Ó 2015 Elsevier B.V. All rights reserved.

1. Introduction Wildfire is a worldwide phenomenon that appears in the geological record soon after the appearance of terrestrial plants (Scott and Glasspool, 2006; Bowman et al., 2009). For hundreds of millions of years, fire influences global ecosystem patterns and processes, helps to shape global biome distribution and to maintain the structure and function of fire-prone communities (Rundel, 1981; Pausas and Vallejo, 1999; Bond and Keeley, 2005; Bond et al., 2005; Bowman et al., 2009; Pausas and Keeley, 2009). Fire also acts as an evolutionary filter against certain plant traits in fire-prone systems (Pausas et al., 2004; Bradshaw et al., 2011; Pausas, 2015). In view of the special role of fire in the ⇑ Corresponding authors. E-mail addresses: [email protected] (W.-H. Su), [email protected] (Z. Shi), [email protected] (R. Zhou), [email protected] (Y.-J. Zhao), [email protected] (G.-F. Zhang).

biosphere, Bond and Keeley (2005) consider fire as a global significant consumer that is analogous to herbivory. Various ecological systems respond differently to fire in their ability to ignite, the intensity and rate-of-spread of fire and their ability to recover after a fire incident (Shlisky et al., 2007; Bowman et al., 2009). Based on natural fire regimes and roles of fire, terrestrial ecosystem can be classified as fire-independent, fire-sensitive and fire-dependent ecosystems (Shlisky et al., 2007). In fire-independent ecosystems such as tundra and deserts, fire is rate, either because of unsuitable climate conditions or lack of biomass to burn (Shlisky et al., 2007; Maezumi et al., 2015). Firesensitive ecosystems such as tropical rainforests are damaged by fire, which disrupts ecological processes that have not evolved with fire (Shlisky et al., 2007; Maezumi et al., 2015). Firedependent ecosystems are those where most of the species have evolved in the presence of fire, and where fire is an essential process for conserving biodiversity, and where fires are natural and plants have the capacity to cope with them (Shlisky et al., 2007).

http://dx.doi.org/10.1016/j.foreco.2015.05.015 0378-1127/Ó 2015 Elsevier B.V. All rights reserved.

Please cite this article in press as: Su, W.-H., et al. The role of fire in the Central Yunnan Plateau ecosystem, southwestern China. Forest Ecol. Manage. (2015), http://dx.doi.org/10.1016/j.foreco.2015.05.015

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Obviously, both fire-sensitive and fire-dependent ecosystems can be the fire-prone habitats, especially under human influence. However, the two different systems should execute different management tactics. Generally, fire-sensitive systems rely on fire suppression, and fire-dependent systems rely on the human application of prescribed fire (Mitchell et al., 2014). The introduction of ecologically-inappropriate fire in fire-sensitive systems can have extensive negative impacts on biodiversity and ecological processes. In Amazon, a typical fire-sensitive system, humanignited wildfires are becoming an increasingly important cause of forest loss (Nepstad et al., 1999; Laurance et al., 2001). It is proved by experiments that anthropogenic understory fires pose a threat to increase tree and liana mortality, reduces biomass and species richness in Amazonian forests (Balch et al., 2008, 2011). Whilst, if fire management policies did not address or even ignore the role of fire in fire-dependent ecosystems, these practices may damage ecological sustainability and lead to ecologically catastrophic fires that burn intensely and may even glassify the soil. In California, one hundred years of fire suppression in a mixed-conifer forest which evolved with frequent natural fires has shifted successional patterns (Parsons and DeBenedetti, 1979). In tall grass prairies fire suppression has led to the loss of as many as 50% of the plant species (Leach and Givnish, 1996; Uys et al., 2004). So it is important to identify the type of the ecosystems with fire regimes. The key difference between the two ecosystems is if the system evolves with fire. In the typical fire-dependent ecosystems such as temperate coniferous forest and savanas, are fire-adapted, flammable and fire-maintained (Pivello, 2011; Maezumi et al., 2015). In these systems, fires remove fine fuels and improve ecological health; meanwhile, fire creates an evolutionary pressure that shape or filter plant traits. Species often exhibit traits such as resprouting, serotiny and germination by heat and smoke. These traits provide species with an ecological fitness and advantage in a fire-prone environment (Bond and Keeley, 2005; Keeley et al., 2011; Pausas, 2015). Re-sprouting commonly occurs in response to injury from a variety of disturbances, including drought, frost, heat wave, waterlogging, herbivory, storm damage, lightning strikes and excessive salt levels (Bond and Midgley, 2001). Different re-sprouting types may have appeared in different plant lineages in response to different evolutionary pressures. However, Keeley et al. (2011) believed that plants with the ability to re-sprout have a fitness advantage in fire-prone habitats. After a fire, fire-tolerant plant species often resprout and grow from protected dormant buds hidden under the bark and in the soil that can survive a fire; second, the resprouting plant can rely on material and energy stored in the original plant, so that re-sprouting occurs far more quickly than the growth of newly germinated seedlings. Serotiny is defined as a condition in which plants retain seeds in the canopy for one to 30 years or more; the high temperature of fire can induce serotinous cones to open and release their seeds after a fire passes through an area (Lamont et al., 1991). Serotinous plants retain a seed bank in the canopy. Compared with seed on the ground, seeds in the canopy are more likely to survive in a forest fire, especially in the case of a ground fire. After a fire, serotinous cones will open and release their seed; these fall to the ground as seed rain. Serotinous cones and canopy seed banks provide serotinous plants with a fitness advantage in fire-prone habitats (Lamont et al., 1991; Lamont and Enright, 2000; Keeley et al., 2011). Serotiny is particularly prominent in Mediterraneanclimate ecosystems of southern Australia, South Africa and the coniferous forests of California, North Africa and the Middle East (Tapias et al., 2004), all of which have fire-prone environments. VerdÚ and Pausas (2007) have suggested that physical dormancy is another trait that reflects a plant’s response to fire; physical dormancy also shows phylogenetic clustering in

Mediterranean plant communities with fire-prone habitats. Seeds undergoing physical dormancy seldom germinate until exposed to the heat shock of a fire (Keeley and Fotheringham, 1997). Observers have seen an enhancement of seed germination by high temperatures between 40 and 70 °C in several fire-prone ecosystems. Fire-cued seed germination occurs as a widespread trait with clear adaptive significance in ecosystems in which a fire may provide space and conditions that are appropriate for the growth of seedling (Tyler and D’ Antonio, 1995; Tyler, 1996; Keeley and Bond, 1997; Keeley and Fotheringham, 1998). Yunnan located in southwestern China and bordering the IndoChina Peninsula in the south, is connected to the Himalayas and Tibet in the northwest (Fig. 1). The mountainous and terraced topography of Yunnan stretches along one of the greatest elevation gradients on earth from 6740 m a.s.l. in the northwest to 76 m a.s.l. in the southeast. The climate ranges from the icy highland of the northwestern frontier to the tropical lowlands of the southern area, with a centrally located subtropical region. There are highly diverse vegetation types ranging from tropical rainforests at lower altitudes and subtropical forests in the central to montane and subalpine temperate forests and alpine meadows at higher altitudes. This is one of the richest areas of biodiversity worldwide. This is a fire-prone region (Li, 2000; Zhao et al., 2009). Actually, the wildfire histories in this area can be traced back to the Later Permian (Shao et al., 2012). From 1961 to 2000, 656 peoples dead from wildfire, every year over 2000 wildfires were reported and 100,000 ha of forests was burnt. The average economic loss directly related to forest wildfires reached over ten million US dollars annually during the past decade (Huo and Liu, 1987; Li, 2000; Zhao et al., 2009). The Central Yunnan Plateau lies in the middle part of this fireprone province (Fig. 1). There are vegetations with a high level of endemicity that is very different from vegetation types typically found in eastern China. The zonal vegetation of Central Yunnan is subtropical semi-humid evergreen broad-leaved forests (henceforth EBLFs) (Wu and Zhu, 1987; Tang and Ohsawa, 2009), while humid EBLFs more typically occur in eastern China. From the global scope, subtropical ecosystem with net primary productivity about 301–600 g C m 2 year 1, are high fire activity (van der Werf et al., 2008; Bowman et al., 2009). In addition, coniferous Pinus yunnanensis forest, an early successional stage in the reestablishment of the EBLFs (Tang, 2010), now dominates a large area (Tang et al., 2010). In the world, most species of the Pinus lineage live in fire-prone ecosystems (Pausas, 2015). Yet relatively little is known about the role of fire in subtropical forest ecosystems in China (Shlisky et al., 2007; Krawchuk and Moritz, 2009; Tang et al., 2013). Which type of this region belongs to? Fire-sensitive or fire-dependent? How to manage fire in these endemicity ecosystems? Although in history fire influences plant evolution, global ecosystem patterns and processes, today fire does not pose a threat to biodiversity or human well-being (Bowman et al., 2009). Therefore, most countries have made fire prevention laws. However, in China, any uncontrolled wildfire that naturally spreads over 100 m2 is termed a ‘‘forest fire disaster” (森林火灾) in documents related to forest fire prevention and management policies. Government and forest management departments must put forth their best efforts to avoid the occurrence of wildfires. Current policies require that once a wildfire occurs it should be extinguished as soon as possible. Are these policies appropriate? This study mainly aims to investigate the fire-adaptive traits of the zonal vegetation in Yunnan’s semi-humid EBLFs and the most widely distributed vegetation type of P. yunnanensis forest and shrub in the Central Yunnan Plateau. The goal is to address the role of fire and determine whether the ecosystems in the Central Yunnan Plateau are fire-sensitive or fire-dependent. Results

Please cite this article in press as: Su, W.-H., et al. The role of fire in the Central Yunnan Plateau ecosystem, southwestern China. Forest Ecol. Manage. (2015), http://dx.doi.org/10.1016/j.foreco.2015.05.015

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Fig. 1. Inset map: the vicinity of the study area within China. Site map: the study area and the location of the ride evaluation and plots investigation of serotiny.

obtained in this study may contribute to revealing the mechanisms that maintain the high biodiversity and community assembly of vegetation endemicity in this area. In addition, the results can guide fire management in the Central Yunnan Plateau. 2. Materials and methods 2.1. Study area The Central Yunnan Plateau lies in the middle part of Yunnan and in Western Yungui Plateau, with a mean elevation of about 2000 m a.s.l. The administrative area of the Central Yunnan Plateau includes Qujing State, Kunming City, Yuxi, City Chuxiong State, Dali State and Lijiang State. The mountainous region and intermountain basin have elevations of 1100–2900 m a.s.l. Controlled by the southwest and southeast monsoons, the region has a plateau monsoon climate characterized by moderately hot, humid summers and warm, dry winters (Chen et al., 2014). The annual mean temperature was 14.6–21.7 °C (1961–1980, data from Yunnan Provincial Meteorological Bureau), the monthly average air temperature was 13.3–24.8 °C and the daily maximum temperature was 25.5–39 °C in March and April. Winter prevails dry continental monsoon, while summer prevails wet marine monsoon, so the distribution of precipitation in the season is very uneven (Chen et al., 2014). Annual precipitation averages between 800 and 1100 mm, and dry season extends from November to April, with 50–130 mm accounting for only 10–20% of annual precipitation. Rainy season extends from May to October, and most precipitation is 6–8 for three months, accounting for about 60% of annual precipitation (Fig. 2). The average annual mean relativity humidity was 54–75%, and was lower (32–65%) in March and April.

Fig. 2. Climate diagram for semi-moist evergreen broad-leaved forest, Kunming, Yunnan, China. After Heinrich Walter, 1985 (date from YCB 1983).

The Central Yunnan Plateau lies within a semi-humid EBLFs region. In the region, the zonal vegetation the semi-humid EBLFs and the early-successional vegetation P. yunnanensis forest are found at elevations ranging from 1600 to 2400 m a.s.l., semisavannas (a vegetation type resembling savannas in appearance distributed in southwestern China (Wu and Zhu, 1987)) below 1600 m a.s.l. and mid-montane moist EBLFs above 2400 m a.s.l.

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This paper focuses on areas with elevations ranging from 1600 to 2400 m a.s.l.

tree as the percentage of closed brown cones out of open and closed cones on the trees.

2.2. Sample plots

2.4.1. Evaluation of serotiny level In P. yunnanensis forest, the distribution of the serotiny level in 80 pine forest plots was sampled over the entire Central Yunnan from August to December, in 2012 and 2013. Three plots were set up for each forest, and each plot distance over 200 m. The years of the oldest opened and closed cone were recorded for each tree. Three main branches from each randomly selected tree were sampled for ten trees in each plot to confirm the ripening year of each closed and open cone for each tree. In January 2013, one closed cone from each cohorts was collected from 30 randomly selected trees in Kunming. All cones of each cohorts were mixed together and dried at 40 °C to release the seed for germination experiments.

We set two types of plots to investigate (Fig. 1): (1) for resrpouting and number of species research at post-fire area with 20  20 m2; (2) for serotiny study with 10  10 m2. The elevation, slope aspect, longitude and latitude were recorded for each plot. The tree height, trunk height, trunk straightness, diameter at breast height (DBH) and number of branches were recorded for each tree in type (2). 2.3. Post-fire re-sprouting and number of species investigation 2.3.1. The re-srpouting and serotiny after fire The re-sprouting and serotiny phenomenon of common species from basal burls was confirmed in the field for five post-fire areas on the 21st and 156th day after fires (Fig. 1). The re-sprouting near a burned tree and shrub base and from the soil was regarded as resprouting from basal burls. Re-sprouting from dormant buds was confirmed based on previously published papers related to resprouting species in shrub communities, which were established after cutting. Four plots were set up in each location, and each plot distance over 500 m. The community table with eight plant community associations, which belong to four formations of semihumid EBLFs, including 80 plots recorded in Yunnan Vegetation (Wu and Zhu, 1987) and Kunming Vegetation (Jin and Peng, 1998) was employed in this study. Any tree species with a frequency greater than 41% in an association, as well as any tall shrubs and other shrubs with a frequency greater than 61%, were regarded as common taxa in the semi-humid EBLFs. If the phenomenon of re-sprouting or serotiny was observed, ‘‘Yes” was recorded; otherwise ‘‘No” was recorded. From April 16 to 19, 2014, a wildfire occurred near Qitai Village, Kunming; pine forest, pine shrubs, tall shrubs of Cyclobalanopsis glaucoides and C. orthacantha were burned in this burned area of about 210 ha. On the 156th day after fire, the condition of sprouting shoot was investigated in this area, including if the sprouting shoots exist and the tall of these shoots. 2.3.2. Post-fire number of species investigation At Qitai location, the number of species during recovering was investigated on the 156th day after fire. Four plots were set up in post-fire area, at the same time four plots of unburned vegetation nearby were set up to compare. Each plot distance over 500 m. 2.4. Serotiny Based on the taxonomic and geographic distributions of serotinous species in previously published papers, Pinus and Cupressus species were most likely to be serotinous (Lamont et al., 1991). In the field, we found some closed cones retained in the canopies of P. yunnanensis; therefore, the potential for serotiny was studied in this species. P. yunnanensis is the most common species and forms the largest forest area in the Central Yunnan Plateau. The seeds of P. yunnanensis require 2 years to mature. The trunk and branch of P. yunnanensis can grow a whorl of shoots every year. The ripening year of each cone can be determined by counting the number of whorls on each trunk and branch. Closed cones (serotinous) and opened cones are easily identified by their different shapes. Serotiny in this study was defined as the proportion of cones, which remained closed after maturation (November). The time of serotiny was calculated for each plot as the age of the oldest closed cones on the trees. The level of serotiny was calculated for each

2.4.2. Investigation of the canopy seed bank structure From August to October, 2013, P. yunnanensis forests (P. yunnanensis var. yunnanensis) were sampled in 6 locations (Kunming, Shuangbai, Shilin, Weishan, Nanhua and Wuding). And the P. yunnanensis shrubs (P. yunnanensis var. pygmaea) were sampled from August to October, 2014 in 3 locations (Kunming, Chuxiong and Mouding). Three plots were set up for each location, and each plot distance over 200 m. Each cone was allocated to a cohorts (ripening year) and status (open or closed) for each tree. 2.5. Heat-shock experiment In January 2013, three closed cones from each crop were collected from 30 randomly selected trees in Chuxiong. All cones from each crop were mixed together and opened by tools to release seeds for a heat shock experiment. The heat shock experiment that was designed to trigger germination; this experiment used methods described for the experiments of Martínez-Sánchez et al. (1995) and Reyes and Casal (2006). Seeds were subjected to three different heat treatments in an oven at 60 °C, 90 °C and 110 °C, for 1, 5 and 15 min, respectively and in sequence. Ten replications of 25 seeds were used for each heat treatment, time exposure and for controls that had no heat treatment. Initially, an empty dish was put into the oven and allowed to equilibrate to the design temperature. Next, 25 seeds were placed in the dish and tested for the selected time. Then, the dish was taken out of the oven; the seeds were moved to another dish at room temperature. Immediately after each heat treatment, seeds were sown in culture bottles and incubated at 1250 Lx light at 21 °C for 8 h followed by dark at 18 °C for 16 h; this light/dark temperature pattern was continued for 45 days. Germination was checked daily and germinated seeds were counted and removed each day during the 45-day period. 2.6. Statistical methods Statistical analysis was done using SPSS 13.0 for Windows (SPSS, Chicago, IL, USA). The significance of difference at P 6 0.05 was assessed by ANOVA. 3. Results 3.1. Re-sprouting In Central Yunnan, zonal vegetation the semi-humid EBLFs consists of four formations dominated by four evergreen trees of the Fagaceae and is distributed at elevations of 1800–2200 m a.s.l. (Wu and Zhu, 1987). All four species of the Fagaceae,

Please cite this article in press as: Su, W.-H., et al. The role of fire in the Central Yunnan Plateau ecosystem, southwestern China. Forest Ecol. Manage. (2015), http://dx.doi.org/10.1016/j.foreco.2015.05.015

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Cyclobalanopsis glaucoides, Castanopsis orthacantha, Castanopsis delavayi and Cyclobalanopsis delavayi, could re-sprout from dormant buds or basal burls (Table 1). In addition, most other common trees, tall shrubs and other shrubs could also re-sprout from dormant buds or basal burls (Table 1). Of 23 common trees, 19 (82.6%) of these species could re-sprout; of 14 tall shrubs, 13 (92.9%) species also could resprout. In addition, most of the 16 common shrubs could all resprout. Overall, about 90.6% of the dominant trees and shrubs could re-sprout. In re-sprouting species, 41 species (77.4% of all species analyzed) could re-sprout from underground basal burls after a fire. 3.2. Post-fire re-sprouting and number of species On the 156th day after fire, sprouting shoots of 12 trees, six tall shrubs and 23 shrubs, and new plants of 16 herbs were found in post-fire land (Fig. 3). Aside from surviving pine trees, all the burned stumps of trees and shrubs (base diameter over 1 cm) had sprouting shoots. New shoots sprouted from the base of stumps and out of the soil near the burned stumps. In the postfire area of land, any pine tree with a burned canopy that did not produce green needles was considered to be dead. However, pine shrubs could sprout from the soil near a burned stump. The longest sprouting shoot was 47 cm long. Compared with unburned vegetation nearby, all trees and tall shrubs were recovered; however, two shrubs and six herbs were lost in the post-fire area of the land (Fig. 3). The recovery rate of trees and tall shrubs were all 100%; those of shrubs and herbs were 93.6% and 73.9%, respectively. 3.3. Serotiny The serotinous cones, which remained closed after maturation were found in all 80 plots of P. yunnanensis forest in the Central Yunnan Plateau, but the time of serotiny was different over all plots (Fig. 4A). In 79% of all plots, closed cones could be retained in the canopy for more than one year; that was, 21% cones opened in the first year (Fig. 4A). In 61% of all plots, trees retained closed cones for 1 or 2 years, and the cones were retained for more than 3 years in 18% of all plots. The longest time a closed cone was retained was for 7 years in the plots investigated in this study. The period of retaining closed cones varied from place to place (Fig. 5). In plots having closed cones, the closed cones accounted for 50.4% of cones retained for 1 and 2 years. The level of serotiny varied from 3% to 100% among 80 plots; the mean level of serotiny among plots was 45.6% ± 25.5. 100% serotiny values were found in 3% and 3.8% of the plots, respectively. The distribution of the level of serotiny among plots was different over all serotiny classes (Fig. 4B). In all the level of serotiny, the 41– 50% classes in which the most plots were found was about 26.3%. Both open and closed cones were retained in the canopy during each ripening year. The percentage of closed cones of the total number of cones that ripened each year varied from place to place (Fig. 5). In most locations, the number of closed cones was greater than the number of open cones in the cones retained for one year. As the year of ripening increased, the percentage of closed cones decreased and that of open cones increased (Fig. 5). The germination rate of seeds (about 90%) was not significantly different among cones retained for 1 and 2 years. As the number of years a cone was retained increased, the germination rate of seeds decreased. After being retained for 7 years, the germination rate for seeds was about 32%. Closed and open cones were present in three sampled population of P. yunnanensis var. pygmaea (Fig. 6). Cones could be retained in the canopy for 5 years; 74.7% of all cones were closed cones retained for 1 and 2 years. Compared with P. yunnanensis var.

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yunnanensis, var. pygmaea was shorter by about 3 m, and had a smaller canopy. Fewer cones per ha were produced in the canopy. The germination rate of seeds retained for 1 and 5 years was 45% and 19%, respectively. 3.4. Heat-shock triggered germination After treatment at 60 °C for 1, 5 and 15 min, seeds of P. yunnanensis var. yunnanensis had higher germination rates than the control by 43.4%, 46.5% and 55.8%, respectively (Fig. 7). After treatment at 90 °C for 1 or 5 min and at 110 °C for 1 min, the germination of seeds was not significantly different from that of the control. After treatment at 90 °C for 15 min and at 110 °C for 5 and 15 min, the germination of seeds was lower than the control (Fig. 7), although there were some live seed among treated seeds. After treatment at 110 °C for 15 min, the seed still had a 36% germination rate. 4. Discussion A fire-dependent ecosystem has two basic characteristics: most of the species have evolved in the presence of periodic fire, and fire plays an essential role in conserving biodiversity (Shlisky et al., 2007). Re-sprouting is one of the significant traits relative with disturbances including fire. On a global scale, semi-humid EBLFs and P. yunnanensis forest types only occur in Southwest China. Many camphor species occur in the humid EBLFs of Eastern China, but only a few occur in semi-humid EBLFs in Southwest China. Oaks, which can re-sprout, are the dominant species in the semi-humid EBLFs (Wu and Zhu, 1987). In the semi-humid EBLFs, all dominant trees, most companion trees and shrubs, and many herbs had sprouting phenomenon (Table 1), account for about 90.6% of the dominant taxa. About 77.4% of all dominant could re-sprout from underground basal burls (Table 1), which were considered to be a special re-sprouting type that evolved under the presence of periodic fire (Keeley et al., 2011). Trees and shrubs in EBLFs would resprout soon after they had burned and most would soon recover after a fire incident. These species belong to different plant taxa, which originated in different regions and distributed in different areas; all are capable of re-sprouting although re-sprouting sometimes occurs through different traits. Re-sprouting is the common trait of most species in the semi-humid EBLFs at the community level. During the process of community assembly, the environment may serve as a filter, which removes all species lacking specific traits. This allows the species to adapt to the key disturbances or pressures, and causes those species in the community to have traits allowing them to adapt to local conditions. This environmental filter increases species similarity in certain characteristics through abiotic constraints (Weiher and Keddy, 1995; Cornwell et al., 2006). Community assembly processes are a community level analogue of natural selection (Keddy, 1992). Fire serves as a strong community assembling process in fire-prone environments, filtering the species that have fire-tolerant traits; species that lack traits that bestow them with fire-tolerance have not successfully entered the community (Pausas and Verdú, 2008). In the fireprone environment of the Central Yunnan Plateau, aside from fire disturbance, other types of disturbance do not damage all trees, shrubs and herbs. Meanwhile, aside from fire disturbance, other disturbances could not explain why re-sprouting is a community level trait for the semi-humid EBLFs. Based on the re-sprouting trait, we believe that fire disturbance plays an important role in community assembly for the semi-humid EBLFs. Perhaps the resprouting traits of plants in the semi-humid EBLFs per se did not originate in response to fire; however, in a fire-prone environment they are ‘exaptations’ (Gould and Vrba, 1982; Keeley et al., 2011) and help the community recover rapidly after fire incidents.

Please cite this article in press as: Su, W.-H., et al. The role of fire in the Central Yunnan Plateau ecosystem, southwestern China. Forest Ecol. Manage. (2015), http://dx.doi.org/10.1016/j.foreco.2015.05.015

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Table 1 Summary of the adaptive traits of dominant taxa in a typical semi-evergreen broad-leaved forest in Central Yunnan Province, China, that have evolved to cope with fire.

a

Scientific name

Growth form

Degree of presence in semi-humid EBLFsa

Resprouting phenomenon after cutting

Resprouting phenomenon from underground basal burls after fire

Serotiny

Castanopsis delavayi Castanopsis orthacantha Cyclobalanopsis delavayi Cyclobalanopsis glaucoides Lithocarpus dealbatus Keteleeria eyelyniana Olea yunnanensis Quercus aliena var. aculeserrata Albizia mollis Cupressus duclouxiana Lithocarpus confinis Lithocarpus craibanus Morus australis Prunus conradinae Pinus armandii Pinus yunnanensis var. yunnanensis Pistacia chinensis Pistacia weinmannifolia Quercus acutissma Quercus variabillis Quercus gilliana Alnus nepalensis Quercus senescens Eurya nitida Lindera communis Lyonia ovalifolia Ternstroemia gymnanthera Toxicodendron succedaneum Vaccinium sprengelii Schima argentea Diospyros mollifolia Pyrus pashia Schoepfia jasminodora Styrax grandiflora Zanthaxylum esquiralii Ilex micrococca Zanthaxylum armatum Fargesia sp. Hypericum uralum Michela yunnanensis Myrsine africana Nothopanax delavayi Pinus yunnanensis var. pygmaea Rhododendron microphyton Rhododendron spinuliferum Smilax siderophylla Camellia reticulata Campylotropis polyantha Elsholtzia rugulosa Reinwardtia indica Rhododendron decorum Rhamnus virgatus Vaccinium figile

Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tree Tall shrub Tall shrub Tall shrub Tall shrub Tall shrub Tall shrub Tall shrub Tall shrub Tall shrub Tall shrub Tall shrub Tall shrub Tall shrub Tall shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub Shrub

V V V V V V V IV III III III III III III III III III III III III III II II V V V V V V IV III III III III III II II V V V V V V V V V IV IV IV IV IV IV IV

Yes Yes Yes Yes Yes Yes Yes Yes Yes No Yes Yes Yes Yes No No Yes Yes Yes Yes Yes No Yes Yes Unconfirmed Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes

Yes Yes Yes Yes Yes Yes Yes Yes Yes No Yes Unconfirmed Unconfirmed Unconfirmed No No Yes Yes Yes Yes Yes No Yes Yes Unconfirmed Yes Yes Yes Yes Yes Unconfirmed Yes Yes Yes Yes Yes Yes Yes Yes Yes Yes Unconfirmed Yes Yes Yes Yes Unconfirmed Yes Yes Unconfirmed Yes Yes Yes

No No No No No No No No No Yes No No No No No Yes No No No No No No No No No No No No No No No No No No No No No No No No No No Yes No No No No No No No No No No

I, II, III, IV, and V indicate a range of frequency of each species from most rare (I) to most common (V).

Unlike the pines in eastern China, the pines of this area (P. yunnanensis including P. yunnanensis var. yunnanensis and var. pygmaea) are serotinous species. The ripe seeds of P. yunnanensis were retained in the plant canopy for 1 to 7 years in the canopy seed bank. Serotiny is believed to be an adaptation to high intensity canopy fires. Serotinous species are dominant flora of fireprone areas (Lamont et al., 1991). Serotinous species can be divided into two groups, strongly and weakly serotinous. Strongly serotinous plants retain most seeds for a few years, and seeds are released after a fire. Weakly serotinous plants lose most seeds within a few years even without fire (Lamont et al., 1991). Some serotinous cones retain in the canopy of P. yunnanensis opened to release some seeds without fire. P. yunnanensis is a weakly serotinous species, which evolved in a way that allows them to cope with fire (Tapias et al., 2001; Briand et al., 2015).

Two regeneration patterns help various species in overcoming hazards created by wildfires, re-sprouting after fire and the stimulation of recruitment by fire. Fire stimulates recruitment in those species in which seed dispersal, germination, flowering, etc. are stimulated or facilitated by heat or smoke (Naveh, 1975). Germination that is stimulated by heat (high temperature) has been termed heat shock (Gifford and Taleisnik, 1994; Gashaw and Michelsen, 2002; Ribeiro et al., 2013). Serotinous cones of P. yunnanensis could be induced to open by high temperatures; high temperatures (60 °C) also resulted in increased germination rates for seeds of P. yunnanensis, as was also found in Mediterranean pines, P. halepensis and P. pinaster (Martínez-Sánchez et al., 1995). Typically, in mature P. yunnanensis forests (P. yunnanensis var. yunnanensis) usually occur understory fires. Most mature P. yunnanensis forests are over 20 m tall form monolayer forests (Xue and

Please cite this article in press as: Su, W.-H., et al. The role of fire in the Central Yunnan Plateau ecosystem, southwestern China. Forest Ecol. Manage. (2015), http://dx.doi.org/10.1016/j.foreco.2015.05.015

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After fire

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Growth form Fig. 3. A comparison of the number of species between post-fire and none-fire plots at Qitai.

Jiang, 2004). Understory fire has little negative influence on mature forests of P. yunnanensis. However we found that canopy fires typically killed all P. yunnanensis trees in an area. Li and Xu (2013) reported that 3 years after a fire in a mixed forest of P. yunnanensis and an evergreen broad-leaf tree (Quercus acutissim), about 15% of the pine trees <10 m tall died, and DBH >15 cm survived. However, the seedlings and saplings of P. yunnanensis grow slowly, reaching a height of about 2–3 m in 10–15 years (Xue and Jiang, 2004), i.e. have a ‘‘grass stage”. A wildfire will kill seedlings and saplings of P. yunnanensis forest (Jin and Peng, 2004). In the fire traits of pines, some enhance fitness in crown-fire ecosystems whereas others increase fitness in ecosystems with understory fires (Pausas, 2015). Generally speaking, ‘‘grass stage” is a trait of fire-tolerator who can survive under frequent understory fire (Pausas, 2015). This is consistent with the observed current fire regime. Meanwhile, serotiny is a typical trait of fire-embracer who suffers crown fires but has mechanisms for quick post-fire recovery of the population (Pausas, 2015). Perhaps the var. yunnanensis is a transition type, which needs more studies. In arid areas with impoverished soils, fire frequency is higher and P. yunnanensis grows more slowly making it difficult for mature forests of P. yunnanensis to become established. In this kind of area, a kind of pine shrubland, the P. yunnanensis var. pygmaea community (Jin and Peng, 2004), can be found. Var. pygmaea has no main trunk, but is more branched than a typical tree. It grows into a shrub, so that the height of the community remains rather low, less than 3 m. The regeneration pattern of var. pygmaea is different from var. yunnanensis and other pines in China. Var. yunnanensis can re-sprout after a fire from basal burls in the soil. This kind of re-sprouting was a typical trait that evolved under fire disturbance (Keeley et al., 2011). Even if fire destroys the aboveground part of the plant, var. pygmaea can recover by re-sprouting. Var. pygmaea is a serotinous variety,

30

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Raletivity frequency (%)

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25 20 15 10 5 0

and retains a canopy seed bank much like var. yunnanensis. Var. pygmaea is differentiated from var. yunnanensis and evolves with the ability to cope with fire. The morphology and traits of var. pygmaea are similar with fire-embracer (Pausas, 2015). In theory, P. yunnanensis forest should succeed to semihumid EBLFs, although disturbance may interrupt forest succession. The Clementsian view of orderly succession to a stable climax community might not be applicable to fire-prone ecosystems (Hanes, 1971). It is suggest that in the Central Yunnan Plateau the distribution pattern of vegetation, including a large area dominated by coniferous P. yunnanensis forest, is not a strongly human-modified landscape where natural EBLFs were exploited destructively and replaced by coniferous P. yunnanensis forest; perhaps these are natural landscapes in a fireprone environment. However, this hypothesis needs more investigations. Based on the fire history and number of fires reported here annually, the Central Yunnan Plateau area is a fire-prone environment. Dominant and common taxa in the typical forests of this region have typical traits and adaptations of plants that are naturally adapted to periodic fire, including the ability to re-sprout from basal burls in soil, serotiny and germination by heat. Even though it cannot be proven that those traits evolved to cope with fire per se, they do provide the local species with a competitive advantage in a fire-prone environment. In the Central Yunnan Plateau, the zonal vegetation and the early successional vegetation have obvious adaptations to periodic fire, they can recover after fire, and forest fire do not significantly reduce number of species. Based on the above results, the Central Yunnan Plateau ecosystem is a fire-dependent system. Wildfire plays an important role in the community assembly for the semi-humid EBLFs, P. yunnanensis forest and shrub. In the Central Yunnan Plateau wildfire should not be considered a total disaster. The current forest fire prevention and management policies, which were developed in Eastern China, would lead to ecological problems if they were aggressively applied to manage wildfire in the Central Yunnan Plateau ecosystem. In Yunnan, the forest managers and researchers as early as 1990s had realized that removing fuels was an effective pathway to prevent wildfire. They attempted to introduce prescribed burning in fire management, and had carried out some practical and research works (Xiong, 2010). In 2009, the local government issued a procedure of prescribed burning. However, due to lack of understanding about the positive role of fire in the area, trapped in the fear of loss of biodiversity, the actual applications of prescribed burning are very limited. The results of this study show that the forests in this region have ecological adaptability of fire, so in theory it is appropriate to carry out the prescribed burning.

<1

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Range of serotiny time (year)

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B

25 20 15 10 5 0

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20

30

40

50

60

70

80

90 100

Range of senotiny level (%)

Fig. 4. The distribution among the range of the time (A) and the level (B) of serotiny in 80 plots.

Please cite this article in press as: Su, W.-H., et al. The role of fire in the Central Yunnan Plateau ecosystem, southwestern China. Forest Ecol. Manage. (2015), http://dx.doi.org/10.1016/j.foreco.2015.05.015

Weishan

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Fig. 5. Variation of number of open and closed cones for Pinus yunnanensis var. yunnanensis per ha units with ripening year of cones (mean ± SD).

Kunming

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3 2.5 2 1.5 1 0.5 0

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Chuxiong 3 2.5 2 1.5 1 0.5 0

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Ripening year of cones

Fig. 6. Variation in the number of open and closed cones for Pinus yunnanensis var. pygmaea per ha units with the ripening year of the cones (mean ± SD).

Germination percentage (%)

1min 100 90 80 70 60 50 40 30 20 10 0

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c c b

b a

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Treatments Fig. 7. Percentage germination of Pinus yunnanensis var. yunnanensis seeds in the original situation and after thermal shock treatments: 60 °C, 90 °C, 110 °C and exposure times of 1, 5 and 15 min (Mean ± SD). Different letters denote significantly difference at P < 0.05.

Acknowledgements The National Natural Science Foundation (31160092) supported this research. The authors thank Feng-Tao Cui and Yuan-Xia Chang for field and laboratory assistance. References Balch, J.K., Nepstad, D.C., Brando, P.M., Curran, L.M., Portela, O., De Carvalho, O., Lefebvre, P., 2008. Negative fire feedback in a transitional forest of southeastern Amazonia. Global Change Biol. 14, 2276–2287.

Balch, J.K., Nepstad, D.C., Curran, L.M., Brando, P.M., Portela, O., Guilherme, P., Reuning-Scherer, J.D., de Carvalho Jr., O., 2011. Size, species, and fire behavior predict tree and liana mortality from experimental burns in the Brazilian Amazon. For. Ecol. Manage. 261, 68–77. Bond, W.J., Keeley, J.E., 2005. Fire as a global ‘herbivore’: the ecology and evolution of flammable ecosystems. Trends Ecol. Evol. 20, 387–394. Bond, W.J., Midgley, J.J., 2001. Ecology of sprouting in woody plants: the persistence niche. Trends Ecol. Evol. 16, 45–51. Bond, W.J., Woodward, F.I., Midgley, G.F., 2005. The global distribution of ecosystems in a world without fire. New Phytol. 165, 525–538. Bowman, D.M.J.S., Balch, J.K., Artaxo, P., Bond, W.J., Carlson, J.M., Cochrane, M.A., D’Antonio, C.M., DeFries, R.S., Doyle, J.C., Harrison, S.P., Johnston, F.H., Keeley, J. E., Krawchuk, M.A., Kull, C.A., Marston, J.B., Moritz, M.A., Prentice, I.C., Roos, C.I., Scott, A.C., Swetnam, T.W., van der Werf, G.R., Pyne, S.J., 2009. Fire in the earth system. Science 324, 481–484. Bradshaw, S.D., Dixon, K.W., Hopper, S.D., Lambers, H., Turner, S.R., 2011. Little evidence for fire-adapted plant traits in Mediterranean climate regions. Trends Plant Sci. 16, 69–76. Briand, C., Schwilk, D., Gauthier, S., Bergeron, Y., 2015. Does fire regime influence life history traits of jack pine in the southern boreal forest of Québec, Canada? Plant Ecol. 216, 157–164. Chen, F., Fan, Z., Niu, S., Zheng, J., 2014. The influence of precipitation and consecutive dry days on burned areas in Yunnan Province, Southwestern China. Adv. Meteorol. 2014, 11. Cornwell, W.K., Schwilk, D.W., Ackerly, D.D., 2006. A trait-based test for habitat at filtering: convex hull volume. Ecology 87, 1465–1471. Gashaw, M., Michelsen, A., 2002. Influence of heat shock on seed germination of plants from regularly burnt savanna woodlands and grasslands in Ethiopia. Plant Ecol. 159, 83–93. Gifford, D.J., Taleisnik, E., 1994. Heat-shock response of Pinus and Picea seedlings. Tree Physiol. 14, 103–110. Gould, S.J., Vrba, E.S., 1982. Exaptation – a missing term in the science of form. Paleobiology 8, 4–15. Hanes, T.L., 1971. Succession after fire in the chaparral of Southern California. Ecol. Monogr. 41, 27–52. Huo, Z., Liu, H.N., 1987. The characteristics of forest fire in Yunnan province. Forest Fire Prevent., 12–14 Jin, Z.-Z., Peng, J., 1998. Vegetation of Kunming. Yunnan Science and Technology Press, Kunming.

Please cite this article in press as: Su, W.-H., et al. The role of fire in the Central Yunnan Plateau ecosystem, southwestern China. Forest Ecol. Manage. (2015), http://dx.doi.org/10.1016/j.foreco.2015.05.015

W.-H. Su et al. / Forest Ecology and Management xxx (2015) xxx–xxx Jin, Z.-Z., Peng, J., 2004. Pinmus yunnanensis forest. Yunnan Science and Technology Press, Kunming. Keddy, P.A., 1992. Assembly and response rules: two goals for predictive community ecology. J. Veg. Sci. 3, 157–164. Keeley, J., Bond, W., 1997. Convergent seed germination in South African fynbos and Californian chaparral. Plant Ecol. 133, 153–167. Keeley, J.E., Fotheringham, C.J., 1997. Trace gas emissions and smoke-induced seed germination. Science 276, 1248–1250. Keeley, J.E., Fotheringham, C.J., 1998. Mechanism of smoke-induced seed germination in a post-fire chaparral annual. J. Ecol. 86, 27–36. Keeley, J.E., Pausas, J.G., Rundel, P.W., Bond, W.J., Bradstock, R.A., 2011. Fire as an evolutionary pressure shaping plant traits. Trends Plant Sci. 16, 406–411. Krawchuk, M.A., Moritz, M.A., 2009. Fire regimes of China: inference from statistical comparison with the United States. Global Ecol. Biogeogr. 18, 626–639. Lamont, B.B., Enright, N.J., 2000. Adaptive advantages of aerial seed banks. Plant Species Biol. 15, 157–166. Lamont, B., Le Maitre, D.C., Cowling, R.M., Enright, N.J., 1991. Canopy seed storage in woody plants. Bot. Rev. 57, 277–317. Laurance, W.F., Cochrane, M.A., Bergen, S., Fearnside, P.M., Delamônica, P., Barber, C., D’Angelo, S., Fernandes, T., 2001. The future of the Brazilian Amazon. Science 291, 438–439. Leach, M.K., Givnish, T.J., 1996. Ecological determinants of species loss in remnant prairies. Science 273, 1555–1558. Li, G., 2000. Forest fire causes analysis and management countermeasures in Yunnan province. Forest Fire Prevent., 10–11 Li, T.-X., Xu, J.-D., 2013. Natural regeneration of mixed conifer and broadleaved forest on the post-fire land in the central Yunnan. Jiangsu Agric. Sci. 41, 285– 288. Maezumi, S.Y., Power, M.J., Mayle, F.E., McLauchlan, K., Iriarte, J., 2015. The effects of past climate variability on fire and vegetation in the cerrãdo savanna ecosystem of the Huanchaca Mesetta, Noel Kempff Mercado National Park, NE Bolivia. Clim. Past Discuss. 11, 135–180. Martínez-Sánchez, J.J., Marín, A., Herranz, J.M., Ferrandis, P., De las Heras, J., 1995. Effects of high temperatures on germination of Pinus halepensis Mill. and P. pinaster Aiton subsp. pinaster seeds in southeast Spain. Vegetatio 116, 69–72. Mitchell, R.J., Liu, Y., O’Brien, J.J., Elliott, K.J., Starr, G., Miniat, C.F., Hiers, J.K., 2014. Future climate and fire interactions in the southeastern region of the United States. For. Ecol. Manage. 327, 316–326. Naveh, Z., 1975. The evolutionary significance of fire in the mediterranean region. Vegetatio 29, 199–208. Nepstad, D.C., Verssimo, A., Alencar, A., Nobre, C., Lima, E., Lefebvre, P., Schlesinger, P., Potter, C., Moutinho, P., Mendoza, E., Cochrane, M., Brooks, V., 1999. Largescale impoverishment of Amazonian forests by logging and fire. Nature 398, 505–508. Parsons, D.J., DeBenedetti, S.H., 1979. Impact of fire suppression on a mixed-conifer forest. For. Ecol. Manage. 2, 21–33. Pausas, J.G., 2015. Evolutionary fire ecology: lessons learned from pines. Trends Plant Sci. 20, 318–324. Pausas, J.G., Keeley, J.E., 2009. A burning story: the role of fire in the history of life. Bioscience 59, 593–601. Pausas, J., Vallejo, V.R., 1999. The role of fire in European Mediterranean ecosystems. In: Chuvieco, E. (Ed.), Remote Sensing of Large Wildfires. Springer, Berlin Heidelberg, pp. 3–16. Pausas, J.G., Verdú, M., 2008. Fire reduces morphospace occupation in plant communities. Ecol. – Ecol. Soc. Am. 89, 2181–2186. Pausas, J.G., Bradstock, R.A., Keith, D.A., Keeley, J.E., 2004. Plant functional traits in relation to fire in crown-fire ecosystems. Ecology 85, 1085–1100. Pivello, V.R., 2011. The use of fire in the Cerrado and Amazonian rainforests of Brazil: past and present. Fire Ecol. 7, 24–39.

9

Reyes, O., Casal, M., 2006. Seed germination of Quercus robur, q. pyrenaica and q. ilex and the effects of smoke, heat, ash and charcoal. Ann. For. Sci. 63, 205–212. Ribeiro, L.C., Pedrosa, M., Borghetti, F., 2013. Heat shock effects on seed germination of five Brazilian savanna species. Plant Biol. 15, 152–157. Rundel, P.W., 1981. Fire as an ecological factor. In: Lange, O.L., Nobel, P.S., Osmond, C.B., Ziegler, H. (Eds.), Physiological Plant Ecology I. Springer, Berlin Heidelberg, pp. 501–538. Scott, A.C., Glasspool, I.J., 2006. The diversification of Paleozoic fire systems and fluctuations in atmospheric oxygen concentration. Proc. Natl. Acad. Sci. 103, 10861–10865. Shao, L., Wang, H., Yu, X., Lu, J., Zhang, M., 2012. Paleo-fires and atmospheric oxygen levels in the latest Permian: evidence from maceral compositions of coals in Eastern Yunnan, Southern China. Acta Geol. Sin. – English Ed. 86, 949–962. Shlisky, A., Waugh, J., Gonzalez, P., Gonzalez, M., Manta, M., Santoso, H., Alvarado, E., Nuruddin, A.A., Rodríguez-Trejo, D.A., Swaty, R., Schmidt, D., Kaufmann, M., Myers, R., Alencar, A., Kearns, F., Johnson, D., Smith, J., Zollner, D., 2007. Fire, ecosystems & people: threats and strategies for global biodiversity conservation. In, Global Fire Initiative Technical Report 2007–2. The Nature Conservancy. Tang, C.Q., 2010. Subtropical montane evergreen broad-leaved forests of Yunnan, China: diversity, succession dynamics, human influence. Front. Earth Sci. China 4, 22–32. Tang, C.Q., Ohsawa, M., 2009. Ecology of subtropical evergreen broad-leaved forests of Yunnan, southwestern China as compared to those of southwestern Japan. J. Plant Res. 122, 335–350. Tang, C.Q., Zhao, M.-H., Li, X.-S., Ohsawa, M., Ou, X.-K., 2010. Secondary succession of plant communities in a subtropical mountainous region of SW China. Ecol. Res. 25, 149–161. Tang, C.Q., He, L.-Y., Su, W.-H., Zhang, G.-F., Wang, H.-C., Peng, M.-C., Wu, Z.-L., Wang, C.-Y., 2013. Regeneration, recovery and succession of a Pinus yunnanensis community five years after a mega-fire in central Yunnan, China. For. Ecol. Manage. 294, 188–196. Tapias, R., Gil, L., Fuentes-Utrilla, P., Pardos, J.A., 2001. Canopy seed banks in Mediterranean pines of south-eastern Spain: a comparison between Pinus halepensis Mill., P. pinaster Ait., P. nigra Arn. and P. pinea L. J. Ecol. 89, 629–638. Tapias, R., Climent, J., Pardos, J., Gil, L., 2004. Life histories of Mediterranean pines. Plant Ecol. 171, 53–68. Tyler, C.M., 1996. Relative importance of factors contributing to postfire seedling establishment in maritime chaparral. Ecology 77, 2182–2195. Tyler, C., D’ Antonio, C., 1995. The effects of neighbors on the growth and survival of shrub seedlings following fire. Oecologia 102, 255–264. Uys, R.G., Bond, W.J., Everson, T.M., 2004. The effect of different fire regimes on plant diversity in southern African grasslands. Biol. Conserv. 118, 489–499. van der Werf, G.R., Randerson, J.T., Giglio, L., Gobron, N., Dolman, A.J., 2008. Climate controls on the variability of fires in the tropics and subtropics. Global Biogeochem. Cycles 22, n/a–n/a. VerdÚ, M., Pausas, J.G., 2007. Fire drives phylogenetic clustering in Mediterranean Basin woody plant communities. J. Ecol. 95, 1316–1323. Weiher, E., Keddy, P.A., 1995. The assembly of experimental wetland plant communities. Oikos 73, 323–335. Wu, Z.-Y., Zhu, Y.-C., 1987. The Vegetation of Yunnan. Science Press, Beijing. Xiong, S.K., 2010. Forest fire occurrence and fire prevention measures in Qujing. Forest Inventory Planning 35 (96–98), 102. Xue, J.-R., Jiang, H.-Q., 2004. Yunnan Forest. Yunnan Science and Technology Press, Kunming. Zhao, F.-J., Shu, L.-F., Tiao, X.-R., Wang, M.-Y., 2009. Change trends of forest fire danger in Yunnan Province in 1957–2007. Chin. J. Ecol. 28, 2333–2338.

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