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Short-term dynamic shifts in woody plants in a montane mixed evergreen and deciduous broadleaved forest in central China
Forest Ecology and Management 310 (2013) 740–746
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Short-term dynamic shifts in woody plants in a montane mixed evergreen and deciduous broadleaved forest in central China Jielin Ge a,b, Gaoming Xiong a, Changming Zhao a, Guozhen Shen a, Zongqiang Xie a,⇑ a b
State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, No. 20 Nanxincun, Xiangshan, Beijing 100093, China University of Chinese Academy of Sciences, Beijing 100049, China
a r t i c l e
i n f o
Article history: Received 10 June 2013 Received in revised form 10 September 2013 Accepted 11 September 2013 Available online 4 October 2013 Keywords: Successional groups Size distributions Ice storm Permanent plot Demographics Mortality
a b s t r a c t The composition and structure in many forests is drifting across the world, although the causes of these changes remain unclear. We studied species turnover, mortality and recruitment, and population dynamism for different successional groups based on three datasets collected between 2001 and 2010 from a permanent 120 m 80 m plot in a Fagus engleriana–Cyclobalanopsis multinervis mixed forest patch in central China, to identify trends in forest change and explore the possible effects of ice storm in 2008 on forest dynamics. The majority of woody species in this forest belonged to early- and late-successional species and the proportion of evergreen species was lower than that of deciduous in terms of species richness. Floristic composition showed minor structural and compositional changes with no shift in the rank of importance value index among different successional groups, over the study periods, whereas stem density and basal area changed markedly between 2006 and 2010, probably as a consequence of the ice storm in 2008. Size distributions of living individuals were similar between census intervals for all successional groups, approximating an inverse J-shaped distribution for early- and late-successional species groups and a bell-shaped distribution for pioneer species, whereas size distributions of dead individuals varied significantly for all successional groups. Furthermore, patterns of mortality and recruitment displayed disequilibrium behaviors over the investigated period with mortality surpassing recruitment for all successional groups during the final census. Surprisingly, diameter growth rates reached a maximum during the final census interval (2006–2010) among all successional groups. All successional groups also showed size-dependent growth with maximal growth rates attained among the largest-sized classes except for pioneer species, which exhibited the highest growth rates at mid-sized classes. Moreover, icestorm in 2008 also accelerated dynamisms among successional groups to different extents. The dynamism gauged by stem density was significantly lower than that based on basal area among successional groups during 2001–2006 but the reverse situation was observed in the later census interval, demonstrating the divergence in diameter growth rate but not in recruitment individuals between the two census intervals made large contribution to this observation. Taken together, these results indicate that despite the 2008 ice-storm this forest was generally resilient, undergoing only minor structural and compositional shifts, although an accelerated rate of forest dynamism among successional groups was linked to the period that included the ice storm. Therefore, long-term observation is needed to further reveal direct evidence of relationships between disturbance and forest dynamics. Ó 2013 Elsevier B.V. All rights reserved.
1. Introduction The understanding of forest dynamics or turnover is based on measurements of mortality, recruitment and growth rates of individual plants. These demographic parameters are essential for forecasting how forest ecosystem may respond to global climatic change (Phillips and Gentry, 1994; Fauset et al., 2012) and extreme climatic events (Condit et al., 1992; Lloret et al., 2012).The issue is
⇑ Corresponding author. Tel./fax: +86 10 62836284. E-mail address: [email protected] (Z. Xie). 0378-1127/$ - see front matter Ó 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.foreco.2013.09.019
particularly significant when conceptualizing forest conservation and management strategies (Hubbell and Foster, 1992). Long-term vegetation monitoring has been undertaken in various forests around the world, particularly in tropical areas (Rees et al., 2001; Laurance et al., 2004; Feeley et al., 2011; Fauset et al., 2012; Holzmueller et al., 2012; Marimon et al., 2012; van den Berg et al., 2012; Weckel et al., 2006), and an increasing number of studies have shown that forests have undergone dynamic widespread directional shifts in composition and structure (Phillips et al., 2004; Lewis et al., 2009; Enquist and Enquist, 2011; Feeley et al., 2011; Peng et al. 2011; Fauset et al., 2012; Kucbel et al., 2012). In contrast, comparable ecological information for montane
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forests is limited, especially in central China, despite well-established records of floristic composition in this region (Zhao et al., 2005). The capacity for natural disturbances and episodic events to disrupt forest dynamics, shifting structure and community composition have become increasingly apparent in recent years (Takahashi et al., 2003; Woods, 2004; Beaudet et al., 2007; Belote et al., 2012; Holzmueller et al., 2012), with each resident species responding in different ways. Examples of such an extreme, episodic event in this region are infrequent, but often devastating ice storms (Zhou et al., 2013b). Vegetation responses vary widely, depending on both the magnitude and specific timing of these events, in relation to the forest stand structure and species composition (Hooper et al., 2001; Hopkin et al., 2003; Lafon, 2004; Takahashi et al., 2007). While pioneer species may prove most vulnerable to these effects, these events can also allow more resistant latesuccessional species gain a competitive advantage, in response to light gaps, accelerating forest structure and composition advancement toward later successional stages (Lemon, 1961). An alternative proposition is that if damage to the canopy is extensive, the extra light this allows to reach forest floor, permits germination and establishment of pioneer species (Du et al., 2012). Any rapid reproduction and growth of these pioneer species can then retard succession and shift the forest to an earlier successional stage (Siccama et al., 1976). It is therefore essential to try to better understand the range of outcomes associated with ice-storms and how drivers of forest composition. Previous studies on these effects have concentrated on the immediate susceptibility of tree species to ice damage (Hooper et al., 2001; Takahashi et al., 2007). Bragg et al. (2003) and Hopkin et al. (2003); further report how elevation, and topography influence ice deposition, and the associated responses of forest understory seedling or sapling density. To our knowledge, no available studies have systematically investigated the effects of ice storms on the forest successional dynamics with reference to established permanent plots records, as we do here, reporting the impacts of an unprecedented catastrophic ice storm that hit a broad band of subtropical China from 10 January to 6 February 2008. This event caused massive mechanical damage in these natural broad-leaved forests (Stone, 2008), providing a unique opportunity to document the effects of an extreme event on forest dynamics. The montane mixed evergreen and deciduous broadleaved forest is the zonal vegetation type in the northern subtropical zone of China. Literature on the dynamics and ecology of this forest type is scarce and inventory data are limited. This forest displays one of the highest levels of biodiversity in the world and thus is considered extremely vulnerable to global change (Myers et al., 2000). Although human pressure has probably played a major role in the disappearance and fragmentation of these montane forests, climate change is undoubtedly having a major impact on them (Zhao et al., 2005). Our principal objective was to identify how forest dynamics changed during the period from 2001 to 2010, with particular regard to the 2008 ice-storm event. We ask: (1) How was species composition and dominance among successional groups in this forest affected by this event (2) How did the ice storm affect specimen plant size and distributions among successional groups? and (3) Is susceptibility to ice storm different among successional groups?
2. Materials and methods 2.1. Study site The study area was located on the southern slope of the Shennongjia region (31°190 400 N, 110°290 4400 E), north-west of Hubei
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Province, central China. This region is in the transition zone between the subtropical and warm temperate climates, and so it is an important biodiversity conservation hotspot in both China and globally (Myers et al., 2000). The annual precipitation of this area is 1306–1722 mm and the mean annual temperature is ca. 10.6 °C. In 2008, an intense storm occurred in this region. According to weather record of National Field Research Station for Forest Ecosystem in Shennongjia, Hubei, China, located at 1290 m, the snowfall during the storms of January 2008 was 30% higher, minimum daily air temperature was 4 °C lower, and it snowed and/or was misty on twice (up to 28 days) as many days. The trees remained covered with snow and hard rime ice during the storms (Li et al., 2009). At this site, five soil classes conform with elevation: mountain yellow brown soil (600–1500 m), mountain brown soil (1500– 2200 m), mountain dark brown soil (2200–2900 m), brown coniferous forest soil (>2900 m) and mountain meadow soil (>1700 m). Vegetation type also varies along this elevational gradient, from evergreen broad-leaved forests at low elevations to mixed evergreen deciduous broad-leaved forests, mixed coniferous and broad-leaved forests, coniferous forests at higher elevations (Zhao et al., 2005). The zonal vegetation community reported here is F. engleriana–C. multinervis mixed forest, a montane mixed evergreen and deciduous broad-leaved forest. 2.2. Methods 2.2.1. Tree census In order to monitor forest development, a 120 m 80 m permanent plot divided into 96 contiguous 10 m 10 m subplots was established within representative forest patch in 2001. Data were collected following the standard census protocol of the Center for Tropical Forest Science network (Condit, 1998). All woody stems equal to or greater than 4 cm diameter at breast height (dbh) were identified, labeled and mapped and their dbh were measured to the nearest centimeter. In 2006 and 2010 all tagged individuals were re-censused for dbh and their condition determined (live or dead). For new recruits, those woody stems that had attained 4 cm were identified, tagged and their dbh was measured. 2.2.2. Data analysis Guidance from literature reviews was used principally to classify the species into different successional groups: pioneer, earlyand late-successional species (Appendix A) (Wu, 1980; Peng et al., 1998; Zhang and Chen, 2000; Xiong et al., 2002; Yu et al., 2002). Analyses included: (1) floristic changes including stem number, basal area and mean stem diameter; (2) turnover (mortality and recruitment); (3) size distributions of living and dead individuals; (4) diameter growth rate; and (5) dynamism. Importance Value Index (IVI) for the different successional groups was calculated as followed: IVI = [relative density + relative basal area + relative frequency]/3 100 (Lévesque et al., 2011); the annualized rate of mortality (m) and recruitment (r) following the standard models: m = (ln(N0) ln(Ns))/t 100; r = (ln(Nt) ln(Ns))/t 100; where Nt and N0 represent the size of the successional group at time t and time 0, respectively, and Ns represents the number of survivors at time t (Laurance et al., 2004). Specific successional group dynamism (D) was calculated as the average of the recruitment (r) and mortality (m) for the study period. Half-life time (t0.5), the time that would take for a given successional group to lose 50% of all its individuals, was calculated as follows: t0.5 = (ln0.5)/ln(1 m) (Cascante-Marín et al., 2011), and double-time (t2), as the time that specific successional group take to double, expressed: t2 = ln(2)/ln(1 + r) (Saiter et al., 2011). The turnover time and stability time were obtained from the mean
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disappeared although there was no new addition of new species through recruitment. IVI for each successional groups shifted gradually over time and late-successional species continued to be dominant (Fig. 1). A slight increase in dominance for late-successional species was apparent, while pioneer species showed a slight decline during the study period. Although a decrease in IVI was recorded for the most dominant species except for some early-successional species, such as Toona sinensis, Cornus japonica var. chinensis, Acer griseum, dominant species maintained their positions in the IVI rank whereas rare species experienced some increase in IVI. In addition, both evergreen and deciduous species showed little change in terms of IVI over the course of study period.
Importance Value
80
60
40
20
0 2001
2006
2010
late-successional species pioneer species early successional species
3.2. Stem density and basal area
Fig. 1. Importance value index changes of different successional groups during the study period (2001–2010).
and the numerical difference between t0.5 and t2, respectively (Tanner and Bellingham, 2006). We calculated annualized diameter growth rate for each successional group by dividing the difference in diameter between two consecutive periods by the time in years between the two measurements (Laurance et al., 2004; Zhou et al., 2013a). The differences in size distribution between census intervals among successional groups were analyzed using Kolmogorov-Smirnov tests (Rohner et al., 2012).
3. Results 3.1. Floristic composition The majority of woody species in this forest belonged to earlyand late-successional species and the proportion of evergreen species was lower than that of deciduous species in terms of species richness (Appendix A). No major changes in woody species richness were observed over the nine year period (2001–2010). Two late-successional species (Holboellia fargesii, Toxicodendron radicans) and one early-successional species (Vitis betulifolia) colonized, while no species disappeared from this community during the first census period (2001–2006). However, between 2006 and 2010, one early-successional species (Viburnum rhytidophyllum)
Overall, late-successional species exhibited the highest stem density among different successional groups across the three censuses (Table 1). Stem density of all successional groups changed over the study period, especially between 2006 and 2010. Specifically, pioneer species decreased in stem density from 116 (2001) to 100 (2010) stems/ha while stem density of early- and late-successional species increased gradually in the first five-year period but each declined by 6.0% and 6.3% respectively, during the second census period (Table 1). Furthermore, late-successional species also had the highest basal area among successional groups over time. Basal area increased but varied greatly between 2001 and 2010 (Table 1). This is, basal area of pioneer species increased from 3.09 m2 ha1 in 2001 to 3.25 m2 ha1 in 2006, followed by a slight decrease in 2010 (3.18 m2 ha1); a similar tendency was also recorded for late-successional species, while early-successional species showed a gradual increase in basal area over the study period. Additionally, stem density and basal area for both evergreen and deciduous species increased gradually during the first census period but then declined slightly in 2010, except that deciduous species presented a continuous increase in basal area during the investigation period. 3.3. Mortality and recruitment Based on stem number, we observed relatively low mortality and recruitment rates; however these rates varied substantially among successional groups and between time intervals (Table 2). Between 2001 and 2006, this forest presented relatively low mortality and recruitment rates among successional groups. Pioneer
Table 1 Stem density, basal area and mean stem diameter of different successional groups in a montane mixed evergreen and deciduous broadleaved forest in central China. Basal area (m2 ha1)
Stem density (stems ha1)
Successional group
Pioneer Early-successional Late-successional
Mean stem diameter (cm)
2001
2006
2010
2001
2006
2010
2001
2006
2010
116 702 1855
115 714 1935
100 671 1814
3.09 14.43 21.74
3.25 15.59 23.21
3.18 16.00 22.67
15.78 13.50 10.38
16.33 13.88 10.51
17.41 14.50 10.66
Table 2 Dynamic features of different successional groups based on stem number in a montane mixed evergreen and deciduous broadleaved forest in central China. Successional group
Pioneer Early-successional Late-successional
Recruitment rate (%)
Mortality rate (%)
Dynamism (%)
Half-life time (year)
Double time (year)
Turnover time (year)
Stability time (year)
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
0.623 1.186 0.228
1.323 1.193 1.624
0.36 0.30 0.34
4.49 2.74 3.43
0.49 0.74 0.28
3.01 1.97 2.53
192.19 230.70 203.52
14.43 24.95 19.86
111.61 58.79 304.36
111.61 58.79 304.36
151.9 144.75 253.94
33.58 541.75 31.44
80.59 171.91 100.84
38.31 33.50 23.17
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J. Ge et al. / Forest Ecology and Management 310 (2013) 740–746 Table 3 Dynamic features of different successional groups based on basal area in a montane mixed evergreen and deciduous broadleaved forest in central China. Successional group
Recruitment rate (%)
Mortality rate (%)
Dynamism (%)
Half-life time (year) Double time (year) Turnover time (year)
Stability time (year)
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
1.47 1.87 1.97
0.30 0.12 0.43
1.98 1.23 2.56
0.80 0.90 1.08
1.73 1.55 2.26
232.20 587.65 162.17
34.65 56.23 26.77
53.75 41.75 40.33
232.20 587.65 162.17
142.97 314.70 101.25
41.05 46.82 31.19
178.45 545.90 121.84
12.79 18.82 8.85
Pioneer 1.30 Early-successional 1.67 Late-successional 1.73
40
250
A
2001 2006 2010
200
800
150
600
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400
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200
0
0
C
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B
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Fig. 2. Changes of size distributions of all living individuals among different successional groups during the study period (2001–2010). (A) Pioneer species; (B) early successional species; and (C) late-successional species.
species had a higher mortality rate (0.36%) than early- and latesuccessional species (0.3% and 0.34%) while early-successional species had the highest recruitment rate. Mortality and recruitment rates across different successional groups, however, underwent a radical change between 2006 and 2010. Roughly 12.4% of woody individuals recorded in the 2006 census were dead in the final 2010 census. Pioneer species showed the largest negative balance between recruitment and mortality (3.17%). Early- and late-successional species exhibited the lowest mortality rate (2.74%) and the highest recruitment rate (1.62%). Mortality rates also underwent marked changes with regard to basal area and, along with recruitment rates, exhibited different trends among successional groups (Table 3). Late-successional species showed a higher basal area mortality rate than early-successional species, but early-successional species displayed the highest positive balance over the study period.
3.4. Size distribution Size distributions of living woody individuals varied little between censuses but differed among successional groups (Fig. 2). Over the entire study period, the size distributions of early- and late- successional groups followed approximated an inverse Jshape with many individuals in the small diameter classes while pioneer species showed a bell-shaped with a second peak in the mid-sized classes. Pioneer species had the largest mean stem diameter and all successional groups presented a clear increase in mean stem diameter and a broadening of size distribution over time due to tree growth (Table 1, Fig. 2). There was no significant difference in size distributions between the census periods (p > 0.05). Nevertheless, the relative abundances of different size classes varied among successional groups: stem number in the smaller size classes declined while this increased for the larger size classes over the course of the study. Furthermore, size distributions of dead individuals varied significantly among all successional groups between censuses
(p < 0.05) (Fig. 3). Between 2001 and 2006, there were relatively few dead individuals (1.64% of woody individuals in 2001) across all size classes in all successional groups, as evidenced by the approximately horizontal line, representative of a stochastic mortality pattern. However, during 2006–2010 they followed positive inverse J-shape curve with a higher number of dead individuals in smaller size classes (4–8 cm). 3.5. Diameter growth rates The diameter growth rates for all living individuals became faster between the two census intervals, influenced by both successional groups and size classes. Pioneer species showed the highest diameter growth rate in the two intervals between the three censuses (p < 0.05) (Fig. 4). Furthermore, different size classes exhibited different diameter growth rates: the lowest diameter growth rate was found in the small-sized classes for all successional groups, but the highest growth rate occurred in mid-sized pioneer species classes and in large-sized early- and late-successional classes. 3.6. Forest dynamism Different successional groups in this forest underwent an accelerating rate of change, however dynamism based on stem number was significantly different from that measured by basal area (Tables 2 and 3). Between 2001 and 2006, early-successional species showed the greatest rate of dynamic change in stem number (0.74%) and half-life time (230.7 years) as well as the shortest double time (58.79 years). Between 2006 and 2010, however, pioneer species exhibited greater dynamism and shorter half-life time than early and late-successional species. Basal area patterns among successional groups also evidenced accelerating rates of dynamism as well as half-life time and double time (Table 3). Between 2001and 2006, the basal area dynamism was highest for late-successional species (1.08%), with the shortest
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J. Ge et al. / Forest Ecology and Management 310 (2013) 740–746 12 10
140
B
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40 100
8 30
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0
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50
A
Size class
Fig. 3. Changes of size distributions of dead individuals among different successional groups during the study period (2001–2010). (A) Pioneer species; (B) early successional species; and (C) late-successional species.
half-life time (162.17 years) and double time (40.33 years). By comparison, basal area dynamism for late successional species during the later census interval (2006–2010) was nearly twice that observed during the first census interval (2001–2006).
Although size distributions of different successional groups showed little temporal variation, stem density and basal area among successional groups did exhibit different magnitudes and directions of change during our nine-year study. These significant changes in stem density and basal area occurred between 2006 and 2010, which precipitated by a community-wide mortality and primarily involved small woody individuals. High mortality among small individuals is often observed to affect forest composition (Wyckoff and Clark, 2002; Coomes and Allen, 2007; Mori et al., 2007; Enquist and Enquist, 2011; Lévesque et al., 2011; van den Berg et al., 2012; Zhou et al., 2013a,b). This is believed to be due primarily to suppression caused by larger trees, often evidenced by a high proportion of small standing dead trees. In addition, the ice storm in 2008 was especially destructive of small saplings due snow loading, leading to tree mortality. Consistent with other studies (Enquist and Enquist, 2011), we also found that small individuals appeared less resilient to natural disturbance, being more vulnerable to shade under the closed canopy, and/or to breakage due to branches falling off larger trees, resulting greater higher mortality rates. The storm event, however, did appear to cause a decline in stem density at the small size classes, potentially influencing forest regeneration may have been impacted. Here, prior to the storm saplings were present, but inhibited by low light in the understory, only to be subsequently released by light penetration through canopy cover broken off by ice build up (see also Arii and Lechowicz, 2007).
4. Discussion 4.1. Structural changes among successional groups
There were imbalances between mortality and recruitment rates among successional groups on both census intervals, though 0.40
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2001-2006 2006-2010
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0.35
4.2. Pattern of mortality and recruitment
4-8
0.40
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Diameter growth rate (cm/year)
The composition and structure of forests can often change dramatically after catastrophic events (Holzmueller et al., 2012). By contrast, between censuses two and three, in response to the impact of the substantial ice-storm event in 2008, we noted only minor changes in species richness and IVI among successional groups, with no successional replacement of late-successional species by pioneer species during recovery from ice storm disturbance during the study. Our results are similar to observations reported by a number of studies examining (extreme) environmental effects on tropical and temperate forests (Condit et al., 1992; Mori et al., 2007; Takahashi et al., 2007), that is, these forests might well maintain tree diversity despite extreme climatic perturbations occurring in environmental conditions. The extent of this structural stability likely interacts with the regional species pool, study time span and intensity and timing of disturbance. Indeed, the small changes in floristic composition we noted in this forest over the past nine years could be entirely explained by natural vicissitude, independent of responses to extreme events. Further long-term study will be required to see is this level of forest resilience is maintained over longer periods.
Size class
Fig. 4. Mean diameter growth rates for different successional groups during the study period (2001–2010). (A) Pioneer species; (B) early successional species; and (C) latesuccessional species.
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highly variable. In particular, mortality and recruitment rates underwent substantial changes from pre-2006 rates by the 2010 census, where mortality rates began to exceed recruitment, reversing earlier patterns. This is consistent with other studies, especially relating to pioneer species (Woods, 2000; Mori et al., 2007; Lewis et al., 2009). We speculate that because smaller pioneer species are less resilient to frost, and related mechanical damage, due to lower wood quality, mortality may have exceeded recruitment in this successional class as a direct result of the 2008 ice-storm. To this effect, we may yet observe compensation in recruitment of successional tree classes, as any temporal discontinuity in relative rates resulting from the storm plays out (Felfili, 1995; de Souza Werneck and Villaron Franceschinelli, 2004).
could suggest greater resistance to the ice storm effects (Imbert and Portecop, 2008). We conclude that despite the 2008 ice-storm this forest was generally resilient, undergoing only minor structural and compositional shifts, although an accelerated rate of forest dynamism among successional groups was linked to the period that included the ice storm, we cannot exclude that the changes we observed might result independently from natural fluctuations. With the prediction that global change will bring increasing extreme climatic events such ice storms in future (Lloret et al., 2012; Zhou et al., 2013b), resolving the causal relationship between forest dynamics, climatic extremes and resilience to perturbation is imperative for conserving ecosystem integrity.
4.3. Variation in diameter growth rates
Acknowledgements
Contrary to previous findings, that lower growth rates accompany higher mortality among successional groups (Wyckoff and Clark, 2002; Vilà-Cabrera et al., 2011), we found that diameter growth rates among successional groups, over a broad range of plant sizes exhibited a greater increase during the 2006–2010, when mortality increased from pre-2006 rates. One possibility is that the ice storm may have reduced the vigor of woody individuals, findings consistent with other studies (Condit et al., 1992; Olano and Palmer, 2003; Tanner and Bellingham, 2006; Delcamp et al., 2008). Another possibility is that extra light penetrating the canopy, resulting from branch breakage due to ice accumulation, combined with reduced root competition for water and nutrients may have accelerated rates of tree growth. Woody individuals among different successional groups intercept and utilize light in distinct manners (Baker et al., 2003; King et al., 2006). We observed all groups to show size-dependent growth, with the greatest rates attained at larger sizes; except for pioneer species, which had highest growth rates at intermediate sizes. Rates of plant diameter growth are typically greater among taller size classes, since these individuals have better access to light from the canopy (van den Berg et al., 2012) and a larger photosynthetic area (Herault et al., 2011). Because pioneer species are intrinsically short-lived, diameter growth declines with size, due to senescence (Zhou et al., 2013a,b) and other physiological restrictions such as stomatal closure due to longer hydraulic pathways (Koch et al., 2004), and higher respiration load of roots and stems (Herault et al., 2011).
We are grateful to Dr. Chris Newman and Youbin Zhou for valuable comments on an earlier version of this manuscript and Lily Van Eeden for her assistance with English language and grammatical editing of this manuscript. This study was financed by the National Basic Research Program of China (Grant No. 2010CB951301).
4.4. Forest dynamism patterns The determined value of dynamism positioned the studied forest as a substantially dynamic ecosystem among several highly diverse forests. At present, the absence of similar data from other studies prevents further analysis of this tendency for this forest. The forest we observed was relatively dynamic (see Laurance et al., 2010; Shen et al., 2013), especially so in the 2006–2010 interval, where we speculate that the ice storm disturbance may have accelerated dynamics among successional groups with different magnitudes. Two metrics of dynamism differed significantly: prior to 2006 stem density dynamism was significantly lower than that based on basal area among successional groups; however this pattern was reversed during the 2010 census. This suggests that different diameter growth rates, but not recruitment individuals differed between the two censuses sufficiently to eventually accelerate dynamisms among successional groups. Lower dynamism is generally assumed to confer higher resistance to external disturbance (Tanner and Bellingham, 2006). We found that pioneer species exhibited higher diameter growth and balanced mortality and recruitment by the 2010 census, than in previous censuses, which
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Phillips, O.L., Baker, T.R., Arroyo, L., Higuchi, N., Killeen, T., Laurance, W.F., Lewis, S.L., Lloyd, J., Malhi, Y., Monteagudo, A., 2004. Pattern and process in Amazon tree turnover, 1976–2001. Phil. Trans. R. Soc. Lond. B 359, 381–407. Rees, M., Condit, R., Crawley, M., Pacala, S., Tilman, D., 2001. Long-term studies of vegetation dynamics. Science 293, 650. Rohner, B., Bigler, C., Wunder, J., Brang, P., Bugmann, H., 2012. Fifty years of natural succession in Swiss forest reserves: changes in stand structure and mortality rates of oak and beech. J. Veg. Sci. 23, 892–905. Saiter, F.Z., Guilherme, F.A.G., Thomaz, L.D., Wendt, T., 2011. Tree changes in a mature rainforest with high diversity and endemism on the Brazilian coast. Biodivers. Conserv. 20, 1921–1949. Shen, Y., Santiago, L.S., Ma, L., Lin, G.-J., Lian, J.-Y., Cao, H.-L., Ye, W.-H., 2013. Forest dynamics of a subtropical monsoon forest in Dinghushan, China: recruitment, mortality and the pace of community change. J. Trop. Ecol. 29, 131–145. Siccama, T.G., Weir, G., Wallace, K., 1976. Ice damage in a mixed hardwood forest in Connecticut in relation to Vitis infestation. Bull. Torrey Bot. Club 103, 180–183. Stone, R., 2008. Ecologists report huge storm losses in China’s forests. Science 319, 1318. Takahashi, K., Mitsuishi, D., Uemura, S., Suzuki, J.I., Hara, T., 2003. Stand structure and dynamics during a 16-year period in a sub-boreal conifer-hardwood mixed forest, northern Japan. For. Ecol. Manage. 174, 39–50. Takahashi, K.T.K., Arii, K.A.K., Lechowicz, M.J.L.M.J., 2007. Quantitative and qualitative effects of a severe ice storm on an old-growth beech-maple forest. Can. J. For. Res. 37, 598–606. Tanner, E., Bellingham, P., 2006. Less diverse forest is more resistant to hurricane disturbance: evidence from montane rain forests in Jamaica. J. Ecol. 94, 1003– 1010. van den Berg, E., Chazdon, R., Corrêa, B.S., 2012. Tree growth and death in a tropical gallery forest in Brazil: understanding the relationships among size, growth, and survivorship for understory and canopy dominant species. Plant Ecol. 213, 1081–1092. Vilà-Cabrera, A., Martínez-Vilalta, J., Vayreda, J., Retana, J., 2011. Structural and climatic determinants of demographic rates of Scots pine forests across the Iberian Peninsula. Ecol. Appl. 21, 1162–1172. Weckel, M., Tirpak, J.M., Nagy, C., Christie, R., 2006. Structural and compositional change in an old-growth eastern hemlock Tsuga canadensis forest, 1965–2004. For. Ecol. Manage. 231, 114–118. Woods, K.D., 2000. Dynamics in late-successional hemlock-hardwood forests over three decades. Ecology 81, 110–126. Woods, K.D., 2004. Intermediate disturbance in a late-successional hemlocknorthern hardwood forest. J. Ecol. 92, 464–476. Wu, Z.Y., 1980. Vegetation of China. Science Press, Beijing. Wyckoff, P.H., Clark, J.S., 2002. The relationship between growth and mortality for seven co-occurring tree species in the southern Appalachian Mountains. J. Ecol. 90, 604–615. Xiong, X., Xiong, G., Xie, Z., 2002. The regeneration of tree species in the mixed evergreen-deciduous broad-leaved forests in the Shennongjia Mountains, Hubei Province. Acta Ecol. Sin. 22, 2001–2005. Yu, L., Zhu, S., Ye, J., Wei, L., Chen, Z., 2002. Dynamics of a degraded karst forest in the process of natural restoration. Sci. Silvae Sin. 38, 1–7. Zhang, J., Chen, L., 2000. A study on judgment and evaluation of succession situation for a forest community with several dominant tree species in the subtropical zone of China. Sci. Silvae Sin. 36, 116–121. Zhao, C.M., Chen, W.L., Tian, Z.Q., Xie, Z.Q., 2005. Altitudinal pattern of plant species diversity in Shennongjia Mountains, central China. J. Integr. Plant Biol. 47, 1431–1449. Zhou, G., Peng, C., Li, Y., Liu, S., Zhang, Q., Tang, X., Liu, J., Yan, J., Zhang, D., Chu, G., 2013a. A climate change-induced threat to the ecological resilience of a subtropical monsoon evergreen broad-leaved forest in Southern China. Global Change Biol. 19, 1197–1210. Zhou, Y., Newman, C., Chen, J., Xie, Z., Macdonald, D.W., 2013b. Anomalous, extreme weather disrupts obligate seed dispersal mutualism: snow in a sub-tropical forest ecosystem. Global Change Biol. 19, 2867–2877.
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Forest Ecology and Management journal homepage: www.elsevier.com/locate/foreco
Short-term dynamic shifts in woody plants in a montane mixed evergreen and deciduous broadleaved forest in central China Jielin Ge a,b, Gaoming Xiong a, Changming Zhao a, Guozhen Shen a, Zongqiang Xie a,⇑ a b
State Key Laboratory of Vegetation and Environmental Change, Institute of Botany, Chinese Academy of Sciences, No. 20 Nanxincun, Xiangshan, Beijing 100093, China University of Chinese Academy of Sciences, Beijing 100049, China
a r t i c l e
i n f o
Article history: Received 10 June 2013 Received in revised form 10 September 2013 Accepted 11 September 2013 Available online 4 October 2013 Keywords: Successional groups Size distributions Ice storm Permanent plot Demographics Mortality
a b s t r a c t The composition and structure in many forests is drifting across the world, although the causes of these changes remain unclear. We studied species turnover, mortality and recruitment, and population dynamism for different successional groups based on three datasets collected between 2001 and 2010 from a permanent 120 m 80 m plot in a Fagus engleriana–Cyclobalanopsis multinervis mixed forest patch in central China, to identify trends in forest change and explore the possible effects of ice storm in 2008 on forest dynamics. The majority of woody species in this forest belonged to early- and late-successional species and the proportion of evergreen species was lower than that of deciduous in terms of species richness. Floristic composition showed minor structural and compositional changes with no shift in the rank of importance value index among different successional groups, over the study periods, whereas stem density and basal area changed markedly between 2006 and 2010, probably as a consequence of the ice storm in 2008. Size distributions of living individuals were similar between census intervals for all successional groups, approximating an inverse J-shaped distribution for early- and late-successional species groups and a bell-shaped distribution for pioneer species, whereas size distributions of dead individuals varied significantly for all successional groups. Furthermore, patterns of mortality and recruitment displayed disequilibrium behaviors over the investigated period with mortality surpassing recruitment for all successional groups during the final census. Surprisingly, diameter growth rates reached a maximum during the final census interval (2006–2010) among all successional groups. All successional groups also showed size-dependent growth with maximal growth rates attained among the largest-sized classes except for pioneer species, which exhibited the highest growth rates at mid-sized classes. Moreover, icestorm in 2008 also accelerated dynamisms among successional groups to different extents. The dynamism gauged by stem density was significantly lower than that based on basal area among successional groups during 2001–2006 but the reverse situation was observed in the later census interval, demonstrating the divergence in diameter growth rate but not in recruitment individuals between the two census intervals made large contribution to this observation. Taken together, these results indicate that despite the 2008 ice-storm this forest was generally resilient, undergoing only minor structural and compositional shifts, although an accelerated rate of forest dynamism among successional groups was linked to the period that included the ice storm. Therefore, long-term observation is needed to further reveal direct evidence of relationships between disturbance and forest dynamics. Ó 2013 Elsevier B.V. All rights reserved.
1. Introduction The understanding of forest dynamics or turnover is based on measurements of mortality, recruitment and growth rates of individual plants. These demographic parameters are essential for forecasting how forest ecosystem may respond to global climatic change (Phillips and Gentry, 1994; Fauset et al., 2012) and extreme climatic events (Condit et al., 1992; Lloret et al., 2012).The issue is
⇑ Corresponding author. Tel./fax: +86 10 62836284. E-mail address: [email protected] (Z. Xie). 0378-1127/$ - see front matter Ó 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.foreco.2013.09.019
particularly significant when conceptualizing forest conservation and management strategies (Hubbell and Foster, 1992). Long-term vegetation monitoring has been undertaken in various forests around the world, particularly in tropical areas (Rees et al., 2001; Laurance et al., 2004; Feeley et al., 2011; Fauset et al., 2012; Holzmueller et al., 2012; Marimon et al., 2012; van den Berg et al., 2012; Weckel et al., 2006), and an increasing number of studies have shown that forests have undergone dynamic widespread directional shifts in composition and structure (Phillips et al., 2004; Lewis et al., 2009; Enquist and Enquist, 2011; Feeley et al., 2011; Peng et al. 2011; Fauset et al., 2012; Kucbel et al., 2012). In contrast, comparable ecological information for montane
J. Ge et al. / Forest Ecology and Management 310 (2013) 740–746
forests is limited, especially in central China, despite well-established records of floristic composition in this region (Zhao et al., 2005). The capacity for natural disturbances and episodic events to disrupt forest dynamics, shifting structure and community composition have become increasingly apparent in recent years (Takahashi et al., 2003; Woods, 2004; Beaudet et al., 2007; Belote et al., 2012; Holzmueller et al., 2012), with each resident species responding in different ways. Examples of such an extreme, episodic event in this region are infrequent, but often devastating ice storms (Zhou et al., 2013b). Vegetation responses vary widely, depending on both the magnitude and specific timing of these events, in relation to the forest stand structure and species composition (Hooper et al., 2001; Hopkin et al., 2003; Lafon, 2004; Takahashi et al., 2007). While pioneer species may prove most vulnerable to these effects, these events can also allow more resistant latesuccessional species gain a competitive advantage, in response to light gaps, accelerating forest structure and composition advancement toward later successional stages (Lemon, 1961). An alternative proposition is that if damage to the canopy is extensive, the extra light this allows to reach forest floor, permits germination and establishment of pioneer species (Du et al., 2012). Any rapid reproduction and growth of these pioneer species can then retard succession and shift the forest to an earlier successional stage (Siccama et al., 1976). It is therefore essential to try to better understand the range of outcomes associated with ice-storms and how drivers of forest composition. Previous studies on these effects have concentrated on the immediate susceptibility of tree species to ice damage (Hooper et al., 2001; Takahashi et al., 2007). Bragg et al. (2003) and Hopkin et al. (2003); further report how elevation, and topography influence ice deposition, and the associated responses of forest understory seedling or sapling density. To our knowledge, no available studies have systematically investigated the effects of ice storms on the forest successional dynamics with reference to established permanent plots records, as we do here, reporting the impacts of an unprecedented catastrophic ice storm that hit a broad band of subtropical China from 10 January to 6 February 2008. This event caused massive mechanical damage in these natural broad-leaved forests (Stone, 2008), providing a unique opportunity to document the effects of an extreme event on forest dynamics. The montane mixed evergreen and deciduous broadleaved forest is the zonal vegetation type in the northern subtropical zone of China. Literature on the dynamics and ecology of this forest type is scarce and inventory data are limited. This forest displays one of the highest levels of biodiversity in the world and thus is considered extremely vulnerable to global change (Myers et al., 2000). Although human pressure has probably played a major role in the disappearance and fragmentation of these montane forests, climate change is undoubtedly having a major impact on them (Zhao et al., 2005). Our principal objective was to identify how forest dynamics changed during the period from 2001 to 2010, with particular regard to the 2008 ice-storm event. We ask: (1) How was species composition and dominance among successional groups in this forest affected by this event (2) How did the ice storm affect specimen plant size and distributions among successional groups? and (3) Is susceptibility to ice storm different among successional groups?
2. Materials and methods 2.1. Study site The study area was located on the southern slope of the Shennongjia region (31°190 400 N, 110°290 4400 E), north-west of Hubei
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Province, central China. This region is in the transition zone between the subtropical and warm temperate climates, and so it is an important biodiversity conservation hotspot in both China and globally (Myers et al., 2000). The annual precipitation of this area is 1306–1722 mm and the mean annual temperature is ca. 10.6 °C. In 2008, an intense storm occurred in this region. According to weather record of National Field Research Station for Forest Ecosystem in Shennongjia, Hubei, China, located at 1290 m, the snowfall during the storms of January 2008 was 30% higher, minimum daily air temperature was 4 °C lower, and it snowed and/or was misty on twice (up to 28 days) as many days. The trees remained covered with snow and hard rime ice during the storms (Li et al., 2009). At this site, five soil classes conform with elevation: mountain yellow brown soil (600–1500 m), mountain brown soil (1500– 2200 m), mountain dark brown soil (2200–2900 m), brown coniferous forest soil (>2900 m) and mountain meadow soil (>1700 m). Vegetation type also varies along this elevational gradient, from evergreen broad-leaved forests at low elevations to mixed evergreen deciduous broad-leaved forests, mixed coniferous and broad-leaved forests, coniferous forests at higher elevations (Zhao et al., 2005). The zonal vegetation community reported here is F. engleriana–C. multinervis mixed forest, a montane mixed evergreen and deciduous broad-leaved forest. 2.2. Methods 2.2.1. Tree census In order to monitor forest development, a 120 m 80 m permanent plot divided into 96 contiguous 10 m 10 m subplots was established within representative forest patch in 2001. Data were collected following the standard census protocol of the Center for Tropical Forest Science network (Condit, 1998). All woody stems equal to or greater than 4 cm diameter at breast height (dbh) were identified, labeled and mapped and their dbh were measured to the nearest centimeter. In 2006 and 2010 all tagged individuals were re-censused for dbh and their condition determined (live or dead). For new recruits, those woody stems that had attained 4 cm were identified, tagged and their dbh was measured. 2.2.2. Data analysis Guidance from literature reviews was used principally to classify the species into different successional groups: pioneer, earlyand late-successional species (Appendix A) (Wu, 1980; Peng et al., 1998; Zhang and Chen, 2000; Xiong et al., 2002; Yu et al., 2002). Analyses included: (1) floristic changes including stem number, basal area and mean stem diameter; (2) turnover (mortality and recruitment); (3) size distributions of living and dead individuals; (4) diameter growth rate; and (5) dynamism. Importance Value Index (IVI) for the different successional groups was calculated as followed: IVI = [relative density + relative basal area + relative frequency]/3 100 (Lévesque et al., 2011); the annualized rate of mortality (m) and recruitment (r) following the standard models: m = (ln(N0) ln(Ns))/t 100; r = (ln(Nt) ln(Ns))/t 100; where Nt and N0 represent the size of the successional group at time t and time 0, respectively, and Ns represents the number of survivors at time t (Laurance et al., 2004). Specific successional group dynamism (D) was calculated as the average of the recruitment (r) and mortality (m) for the study period. Half-life time (t0.5), the time that would take for a given successional group to lose 50% of all its individuals, was calculated as follows: t0.5 = (ln0.5)/ln(1 m) (Cascante-Marín et al., 2011), and double-time (t2), as the time that specific successional group take to double, expressed: t2 = ln(2)/ln(1 + r) (Saiter et al., 2011). The turnover time and stability time were obtained from the mean
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disappeared although there was no new addition of new species through recruitment. IVI for each successional groups shifted gradually over time and late-successional species continued to be dominant (Fig. 1). A slight increase in dominance for late-successional species was apparent, while pioneer species showed a slight decline during the study period. Although a decrease in IVI was recorded for the most dominant species except for some early-successional species, such as Toona sinensis, Cornus japonica var. chinensis, Acer griseum, dominant species maintained their positions in the IVI rank whereas rare species experienced some increase in IVI. In addition, both evergreen and deciduous species showed little change in terms of IVI over the course of study period.
Importance Value
80
60
40
20
0 2001
2006
2010
late-successional species pioneer species early successional species
3.2. Stem density and basal area
Fig. 1. Importance value index changes of different successional groups during the study period (2001–2010).
and the numerical difference between t0.5 and t2, respectively (Tanner and Bellingham, 2006). We calculated annualized diameter growth rate for each successional group by dividing the difference in diameter between two consecutive periods by the time in years between the two measurements (Laurance et al., 2004; Zhou et al., 2013a). The differences in size distribution between census intervals among successional groups were analyzed using Kolmogorov-Smirnov tests (Rohner et al., 2012).
3. Results 3.1. Floristic composition The majority of woody species in this forest belonged to earlyand late-successional species and the proportion of evergreen species was lower than that of deciduous species in terms of species richness (Appendix A). No major changes in woody species richness were observed over the nine year period (2001–2010). Two late-successional species (Holboellia fargesii, Toxicodendron radicans) and one early-successional species (Vitis betulifolia) colonized, while no species disappeared from this community during the first census period (2001–2006). However, between 2006 and 2010, one early-successional species (Viburnum rhytidophyllum)
Overall, late-successional species exhibited the highest stem density among different successional groups across the three censuses (Table 1). Stem density of all successional groups changed over the study period, especially between 2006 and 2010. Specifically, pioneer species decreased in stem density from 116 (2001) to 100 (2010) stems/ha while stem density of early- and late-successional species increased gradually in the first five-year period but each declined by 6.0% and 6.3% respectively, during the second census period (Table 1). Furthermore, late-successional species also had the highest basal area among successional groups over time. Basal area increased but varied greatly between 2001 and 2010 (Table 1). This is, basal area of pioneer species increased from 3.09 m2 ha1 in 2001 to 3.25 m2 ha1 in 2006, followed by a slight decrease in 2010 (3.18 m2 ha1); a similar tendency was also recorded for late-successional species, while early-successional species showed a gradual increase in basal area over the study period. Additionally, stem density and basal area for both evergreen and deciduous species increased gradually during the first census period but then declined slightly in 2010, except that deciduous species presented a continuous increase in basal area during the investigation period. 3.3. Mortality and recruitment Based on stem number, we observed relatively low mortality and recruitment rates; however these rates varied substantially among successional groups and between time intervals (Table 2). Between 2001 and 2006, this forest presented relatively low mortality and recruitment rates among successional groups. Pioneer
Table 1 Stem density, basal area and mean stem diameter of different successional groups in a montane mixed evergreen and deciduous broadleaved forest in central China. Basal area (m2 ha1)
Stem density (stems ha1)
Successional group
Pioneer Early-successional Late-successional
Mean stem diameter (cm)
2001
2006
2010
2001
2006
2010
2001
2006
2010
116 702 1855
115 714 1935
100 671 1814
3.09 14.43 21.74
3.25 15.59 23.21
3.18 16.00 22.67
15.78 13.50 10.38
16.33 13.88 10.51
17.41 14.50 10.66
Table 2 Dynamic features of different successional groups based on stem number in a montane mixed evergreen and deciduous broadleaved forest in central China. Successional group
Pioneer Early-successional Late-successional
Recruitment rate (%)
Mortality rate (%)
Dynamism (%)
Half-life time (year)
Double time (year)
Turnover time (year)
Stability time (year)
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
0.623 1.186 0.228
1.323 1.193 1.624
0.36 0.30 0.34
4.49 2.74 3.43
0.49 0.74 0.28
3.01 1.97 2.53
192.19 230.70 203.52
14.43 24.95 19.86
111.61 58.79 304.36
111.61 58.79 304.36
151.9 144.75 253.94
33.58 541.75 31.44
80.59 171.91 100.84
38.31 33.50 23.17
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J. Ge et al. / Forest Ecology and Management 310 (2013) 740–746 Table 3 Dynamic features of different successional groups based on basal area in a montane mixed evergreen and deciduous broadleaved forest in central China. Successional group
Recruitment rate (%)
Mortality rate (%)
Dynamism (%)
Half-life time (year) Double time (year) Turnover time (year)
Stability time (year)
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
2001– 2006
2006– 2010
1.47 1.87 1.97
0.30 0.12 0.43
1.98 1.23 2.56
0.80 0.90 1.08
1.73 1.55 2.26
232.20 587.65 162.17
34.65 56.23 26.77
53.75 41.75 40.33
232.20 587.65 162.17
142.97 314.70 101.25
41.05 46.82 31.19
178.45 545.90 121.84
12.79 18.82 8.85
Pioneer 1.30 Early-successional 1.67 Late-successional 1.73
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Fig. 2. Changes of size distributions of all living individuals among different successional groups during the study period (2001–2010). (A) Pioneer species; (B) early successional species; and (C) late-successional species.
species had a higher mortality rate (0.36%) than early- and latesuccessional species (0.3% and 0.34%) while early-successional species had the highest recruitment rate. Mortality and recruitment rates across different successional groups, however, underwent a radical change between 2006 and 2010. Roughly 12.4% of woody individuals recorded in the 2006 census were dead in the final 2010 census. Pioneer species showed the largest negative balance between recruitment and mortality (3.17%). Early- and late-successional species exhibited the lowest mortality rate (2.74%) and the highest recruitment rate (1.62%). Mortality rates also underwent marked changes with regard to basal area and, along with recruitment rates, exhibited different trends among successional groups (Table 3). Late-successional species showed a higher basal area mortality rate than early-successional species, but early-successional species displayed the highest positive balance over the study period.
3.4. Size distribution Size distributions of living woody individuals varied little between censuses but differed among successional groups (Fig. 2). Over the entire study period, the size distributions of early- and late- successional groups followed approximated an inverse Jshape with many individuals in the small diameter classes while pioneer species showed a bell-shaped with a second peak in the mid-sized classes. Pioneer species had the largest mean stem diameter and all successional groups presented a clear increase in mean stem diameter and a broadening of size distribution over time due to tree growth (Table 1, Fig. 2). There was no significant difference in size distributions between the census periods (p > 0.05). Nevertheless, the relative abundances of different size classes varied among successional groups: stem number in the smaller size classes declined while this increased for the larger size classes over the course of the study. Furthermore, size distributions of dead individuals varied significantly among all successional groups between censuses
(p < 0.05) (Fig. 3). Between 2001 and 2006, there were relatively few dead individuals (1.64% of woody individuals in 2001) across all size classes in all successional groups, as evidenced by the approximately horizontal line, representative of a stochastic mortality pattern. However, during 2006–2010 they followed positive inverse J-shape curve with a higher number of dead individuals in smaller size classes (4–8 cm). 3.5. Diameter growth rates The diameter growth rates for all living individuals became faster between the two census intervals, influenced by both successional groups and size classes. Pioneer species showed the highest diameter growth rate in the two intervals between the three censuses (p < 0.05) (Fig. 4). Furthermore, different size classes exhibited different diameter growth rates: the lowest diameter growth rate was found in the small-sized classes for all successional groups, but the highest growth rate occurred in mid-sized pioneer species classes and in large-sized early- and late-successional classes. 3.6. Forest dynamism Different successional groups in this forest underwent an accelerating rate of change, however dynamism based on stem number was significantly different from that measured by basal area (Tables 2 and 3). Between 2001 and 2006, early-successional species showed the greatest rate of dynamic change in stem number (0.74%) and half-life time (230.7 years) as well as the shortest double time (58.79 years). Between 2006 and 2010, however, pioneer species exhibited greater dynamism and shorter half-life time than early and late-successional species. Basal area patterns among successional groups also evidenced accelerating rates of dynamism as well as half-life time and double time (Table 3). Between 2001and 2006, the basal area dynamism was highest for late-successional species (1.08%), with the shortest
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Size class
Fig. 3. Changes of size distributions of dead individuals among different successional groups during the study period (2001–2010). (A) Pioneer species; (B) early successional species; and (C) late-successional species.
half-life time (162.17 years) and double time (40.33 years). By comparison, basal area dynamism for late successional species during the later census interval (2006–2010) was nearly twice that observed during the first census interval (2001–2006).
Although size distributions of different successional groups showed little temporal variation, stem density and basal area among successional groups did exhibit different magnitudes and directions of change during our nine-year study. These significant changes in stem density and basal area occurred between 2006 and 2010, which precipitated by a community-wide mortality and primarily involved small woody individuals. High mortality among small individuals is often observed to affect forest composition (Wyckoff and Clark, 2002; Coomes and Allen, 2007; Mori et al., 2007; Enquist and Enquist, 2011; Lévesque et al., 2011; van den Berg et al., 2012; Zhou et al., 2013a,b). This is believed to be due primarily to suppression caused by larger trees, often evidenced by a high proportion of small standing dead trees. In addition, the ice storm in 2008 was especially destructive of small saplings due snow loading, leading to tree mortality. Consistent with other studies (Enquist and Enquist, 2011), we also found that small individuals appeared less resilient to natural disturbance, being more vulnerable to shade under the closed canopy, and/or to breakage due to branches falling off larger trees, resulting greater higher mortality rates. The storm event, however, did appear to cause a decline in stem density at the small size classes, potentially influencing forest regeneration may have been impacted. Here, prior to the storm saplings were present, but inhibited by low light in the understory, only to be subsequently released by light penetration through canopy cover broken off by ice build up (see also Arii and Lechowicz, 2007).
4. Discussion 4.1. Structural changes among successional groups
There were imbalances between mortality and recruitment rates among successional groups on both census intervals, though 0.40
Size class
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0.10
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0.15
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0.20
0.15
28-32
0.20
0.15
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0.20
20-24
0.25
16-20
0.25
12-16
0.25
8-12
0.30
Size class
C
0.35
0.30
20-24
B
0.35
0.30
8-12
2001-2006 2006-2010
12-16
0.40
A
0.35
4.2. Pattern of mortality and recruitment
4-8
0.40
4-8
Diameter growth rate (cm/year)
The composition and structure of forests can often change dramatically after catastrophic events (Holzmueller et al., 2012). By contrast, between censuses two and three, in response to the impact of the substantial ice-storm event in 2008, we noted only minor changes in species richness and IVI among successional groups, with no successional replacement of late-successional species by pioneer species during recovery from ice storm disturbance during the study. Our results are similar to observations reported by a number of studies examining (extreme) environmental effects on tropical and temperate forests (Condit et al., 1992; Mori et al., 2007; Takahashi et al., 2007), that is, these forests might well maintain tree diversity despite extreme climatic perturbations occurring in environmental conditions. The extent of this structural stability likely interacts with the regional species pool, study time span and intensity and timing of disturbance. Indeed, the small changes in floristic composition we noted in this forest over the past nine years could be entirely explained by natural vicissitude, independent of responses to extreme events. Further long-term study will be required to see is this level of forest resilience is maintained over longer periods.
Size class
Fig. 4. Mean diameter growth rates for different successional groups during the study period (2001–2010). (A) Pioneer species; (B) early successional species; and (C) latesuccessional species.
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highly variable. In particular, mortality and recruitment rates underwent substantial changes from pre-2006 rates by the 2010 census, where mortality rates began to exceed recruitment, reversing earlier patterns. This is consistent with other studies, especially relating to pioneer species (Woods, 2000; Mori et al., 2007; Lewis et al., 2009). We speculate that because smaller pioneer species are less resilient to frost, and related mechanical damage, due to lower wood quality, mortality may have exceeded recruitment in this successional class as a direct result of the 2008 ice-storm. To this effect, we may yet observe compensation in recruitment of successional tree classes, as any temporal discontinuity in relative rates resulting from the storm plays out (Felfili, 1995; de Souza Werneck and Villaron Franceschinelli, 2004).
could suggest greater resistance to the ice storm effects (Imbert and Portecop, 2008). We conclude that despite the 2008 ice-storm this forest was generally resilient, undergoing only minor structural and compositional shifts, although an accelerated rate of forest dynamism among successional groups was linked to the period that included the ice storm, we cannot exclude that the changes we observed might result independently from natural fluctuations. With the prediction that global change will bring increasing extreme climatic events such ice storms in future (Lloret et al., 2012; Zhou et al., 2013b), resolving the causal relationship between forest dynamics, climatic extremes and resilience to perturbation is imperative for conserving ecosystem integrity.
4.3. Variation in diameter growth rates
Acknowledgements
Contrary to previous findings, that lower growth rates accompany higher mortality among successional groups (Wyckoff and Clark, 2002; Vilà-Cabrera et al., 2011), we found that diameter growth rates among successional groups, over a broad range of plant sizes exhibited a greater increase during the 2006–2010, when mortality increased from pre-2006 rates. One possibility is that the ice storm may have reduced the vigor of woody individuals, findings consistent with other studies (Condit et al., 1992; Olano and Palmer, 2003; Tanner and Bellingham, 2006; Delcamp et al., 2008). Another possibility is that extra light penetrating the canopy, resulting from branch breakage due to ice accumulation, combined with reduced root competition for water and nutrients may have accelerated rates of tree growth. Woody individuals among different successional groups intercept and utilize light in distinct manners (Baker et al., 2003; King et al., 2006). We observed all groups to show size-dependent growth, with the greatest rates attained at larger sizes; except for pioneer species, which had highest growth rates at intermediate sizes. Rates of plant diameter growth are typically greater among taller size classes, since these individuals have better access to light from the canopy (van den Berg et al., 2012) and a larger photosynthetic area (Herault et al., 2011). Because pioneer species are intrinsically short-lived, diameter growth declines with size, due to senescence (Zhou et al., 2013a,b) and other physiological restrictions such as stomatal closure due to longer hydraulic pathways (Koch et al., 2004), and higher respiration load of roots and stems (Herault et al., 2011).
We are grateful to Dr. Chris Newman and Youbin Zhou for valuable comments on an earlier version of this manuscript and Lily Van Eeden for her assistance with English language and grammatical editing of this manuscript. This study was financed by the National Basic Research Program of China (Grant No. 2010CB951301).
4.4. Forest dynamism patterns The determined value of dynamism positioned the studied forest as a substantially dynamic ecosystem among several highly diverse forests. At present, the absence of similar data from other studies prevents further analysis of this tendency for this forest. The forest we observed was relatively dynamic (see Laurance et al., 2010; Shen et al., 2013), especially so in the 2006–2010 interval, where we speculate that the ice storm disturbance may have accelerated dynamics among successional groups with different magnitudes. Two metrics of dynamism differed significantly: prior to 2006 stem density dynamism was significantly lower than that based on basal area among successional groups; however this pattern was reversed during the 2010 census. This suggests that different diameter growth rates, but not recruitment individuals differed between the two censuses sufficiently to eventually accelerate dynamisms among successional groups. Lower dynamism is generally assumed to confer higher resistance to external disturbance (Tanner and Bellingham, 2006). We found that pioneer species exhibited higher diameter growth and balanced mortality and recruitment by the 2010 census, than in previous censuses, which
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