Conspecific negative density dependence ... - Wiley Online Library

Conspecific negative density dependence decreases with increasing species abundance MENG XU,1,2 YONGFAN WANG,1

AND

SHIXIAO YU1,

1

Department of Ecology, School of Life Sciences/State Key Laboratory of Biocontrol, Sun Yat-sen University, Guangzhou 510275, China 2 Pearl River Fisheries Research Institute, Chinese Academy of Fishery Sciences, Key Laboratory of Tropical and Subtropical Fishery Resource Application and Cultivation, Ministry of Agriculture, Guangzhou 510380, China Citation: Xu, M., Y. Wang, and S. Yu. 2015. Conspecific negative density dependence decreases with increasing species abundance. Ecosphere 6(12):257. http://dx.doi.org/10.1890/ES15-00144.1

Abstract. Conspecific negative density dependence (CNDD) is often involved in explaining the maintenance of species diversity in forest communities given that it may suppress the common species. Recent studies, in contrast, suggested that CNDD had a stronger effect on rare species than on common species and thus shaped the current tree abundance pattern. However, this finding was obtained mainly in the tropical forest and mixed results also occurred in the similar area. In addition, experimental test of the role of soil biota in maintaining this relationship is rare. In this study, two parallel manipulative shadehouse and field experiments were conducted in a subtropical evergreen broad-leaved forest to test whether abundant species showed weaker CNDD than rarer species and whether susceptibility to soil biota was sufficient to maintain this relationship. The shade-house experiment provided strong evidence for negative density-dependent effects, and the strength of the density effect was significantly decreased along with the increase of the tree abundance. In the field experiment, a similar result was obtained. The density effect did not correlate with tree abundance after the sterilized treatment in the shade-house experiment and the fungicide treatment in the field. Our results indicated that CNDD was negatively corrected with tree abundance in this subtropical forest and that soil biota played an important role in maintaining the relationship. Key words: abundant species; rare species; seedling survival; soil biota; subtropical forest. Received 10 March 2015; revised 4 May 2015; accepted 6 May 2015; published 11 December 2015. Corresponding Editor: D. P. C. Peters. Copyright: Ó 2015 Xu et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. http://creativecommons.org/licenses/by/3.0/ E-mail: [email protected]

INTRODUCTION

dependence pattern is the Janzen-Connell effect, which states that high conspecific seedling density and proximity to conspecific adults reduces seedling survival due to attack by hostspecific enemies (Janzen 1970, Connell 1971). Many previous studies have shown the potentially important roles of soil pathogens (Augspurger 1984, Bever 1994, Mills and Bever 1998, Packer and Clay 2000, Klironomos 2002, Bell et al. 2006, Bradley et al. 2008, Reinhart and Clay

Density-dependent mortality is a frequently proposed mechanism that is used to explain the maintenance of species diversity in forest communities (Wills et al. 1997, Webb and Peart 1999, Harms et al. 2000, Lambers et al. 2002, Volkov et al. 2005, Chen et al. 2010, Metz et al. 2010, Johnson et al. 2012, Comita et al. 2014, Liang et al. 2015). One process underlying the density v www.esajournals.org

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2009, Bagchi et al. 2010, Liu et al. 2012a, b) and insect herbivores (Blundell and Peart 1998, Norghauer et al. 2006, Pigot and Leather 2008, Del-Val and Armesto 2009, Eichhorn et al. 2010) that have been interpreted to contribute to species coexistence. Most of these studies focused on common species (Carson et al. 2008) and presumed that the strong conspecific negative density dependence (CNDD) of the common species would provide space for rare species. If abundant species have many specialized enemies, more common species in the local community may suffer from increased CNDD than the rare species. This would generate a community compensatory trend (CCT) and thus may make species in the community coexist stably (Connell et al. 1984, Webb and Peart 1999, Queenborough et al. 2007). However, two studies in the tropical forests of central Panama and a study in the temperate grassland of Canada revealed that the variations in plant species abundance in these examples may in fact have been a consequence of conspecific negative effects (CNE; Klironomos 2002, Comita et al. 2010, Lewis 2010, Mangan et al. 2010b). The results from these studies showed that rarer species suffered stronger CNDD or negative feedback. In contrast to the expectation that implicitly was derived from earlier renderings of density dependence effects on community structure, that as species become more common, they suffer more from negative density dependence, it now appears that in fact more common species suffer relatively less and that this is directly connected to the fact that they are abundant. A similar conclusion was reached after a recent demographic analysis of the United States Forest Service’s Forest Inventory and Analysis data (Johnson et al. 2012). Specifically, species suffering stronger CNDD are expected to have fewer opportunities to establish near conspecifics, which would potentially limit their relative abundance in the community. In contrast, species experiencing weak CNDD should be able to establish near conspecifics, which would allow them to increase their relative abundance. These studies also viewed the soil biota as the most likely mechanisms underlying these CNE, although resource competition also perhaps a potential cause of them. In contrast to both viewpoints, more recent v www.esajournals.org

studies rejected the hypothesis that measures of soil biota effects can be corrected to demographic pattern (Reinhart 2012, Reinhart et al. 2012a, b), suggesting that complex biotic and abiotic interactions are structuring forests. These authors conducted a serious of manipulative experiments in grassland and forest, calculated the feedback effects and linked them to the tree abundance, yet they did not found the association of soil biota effects and species abundance. These obvious conflicting results require additional studies, particularly in other areas such as subtropical forest, to test the relationship between species abundance and CNE and the potential role of soil biota in maintaining this pattern. In this study, we conducted two parallel manipulative experiments, one in a shade-house and the other in the field. We tested whether negative density dependence varies along species abundance in a subtropical forest in south China, and addressed whether this relationship was mainly maintained by soil biota. In the shadehouse experiment, we examined the variation of density-dependence along different tree species abundance and the effect of soil biota on this relationship through sterilization treatment. We then verified this relationship and using fungicide tested the role of soil biota in the field.

MATERIAL

AND

METHODS

Study site and species All experiments were conducted at the Heishiding Natural Reserve (Guangdong Province, China; 111853 0 E, 23827 0 N, 150–927 m above sea level). The reserve covers 4200 ha of subtropical, evergreen, broad-leaved, monsoon forest. The mean annual temperature is 19.68C, with mean monthly temperatures ranging from 10.68C in January to 28.48C in July. Annual precipitation is 1744 mm on average, with a humid season lasting from April to September and a dry season lasting from October to March. Six 1 ha permanent plots were established during winter 2007 and spring 2008 (Xu and Yu 2014). Five tree species, including Engelhardia fenzelii, Castanopsis fabri, Cryptocarya concinna, Bridelia monoica, and Ormosia glaberrima were selected (Appendix: Table A1). These species were chosen because they vary in abundance and basal area, while the most abundant and rarest species of 2


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our 6 ha survey plots were included. We collected seeds from trees throughout the study site during autumn and winter of 2010. Seeds were surface-sterilized (1 min 70% ethanol, 3 min 50% commercial bleach, 1 min 70% ethanol, and 1 min distilled water) and kept in a refrigerator at 48C until late March 2011. Seeds were left to germinate in plastic boxes filled with soil. Seeds began germinating during the following 4 weeks. We transplanted cultured seedlings of each of our study species to boxes with soil collected from areas near their adults in the shade-house experiment. In the field experiment, we directly transplanted the cultured seedlings of each of the species to soil under their adults. Due to a limited number of seedlings cultured in the shade-house, the first four species were used in the field experiment, while the latter four species were used in the shade-house experiment.

soil biota, we tested seedling survival in the same density treatments using sterilized inoculum. Each density treatment using sterilized inoculum was replicated six times. Density treatments across four species were included as a block. The positions of pots, including species-density combinations, were randomized within the block. The experiment lasted for 24 weeks and seedling survival was determined every 3 weeks (see Appendix: Fig. A1 for the experimental design).

Manipulative field experiment In May 2011, three adult trees of Engelhardia fenzelii, Castanopsis fabri, Cryptocarya and concinna, were randomly located in the subtropical forest, and three trees of Bridelia monoica including two trees (DBH 1 cm) and one adult tree (DBH 10 cm) were chosen given same reason mentioned above (Appendix: Table A1). Two 1.4 3 1 m test plots were established 1 m away from the base of each tree. One plot was treated with fungicide, and the other plot was sprayed with the same amount of water as a control. Two plots were separated by a distance of 0.5 m to preventing the potential drift of fungicide. Each plot was divided into five subplots (1.4 3 0.2 m). Two subplots on both sides were divided into seven test squares (0.2 3 0.2 m). The three middle subplots were left as a buffer zone to separate the density treatments. For each plot of each species, one conspecific seedling was planted in the central area of each square of one side subplot, and four conspecific seedlings were planted in each square of the other side (70 seedlings total for each tree of each species and 35 seedlings for each plot). Two types of fungicides were alternatively applied as a spray every 2 weeks, in accordance with the manufacturers’ recommendations: 2.0 g m2 of Captan WP and 1.0 g m2 of metalaxyl-mancozeb (8% metalaxyl and 64% mancozeb), with 800 mL of solution applied to 1 m2. The field experiment lasted 24 weeks, and seedling survival was determined every 2 weeks during the first 4 weeks and every 5 weeks until the end of the experiment (see Appendix: Fig. A2 for the experimental design).

Shade-house experiment Four adult trees of Castanopsis fabri, Cryptocarya concinna and Ormosia glaberrima were chosen as inoculum sources, and four trees of Bridelia monoica including three trees (DBH 1 cm) and one adult tree (DBH 10 cm) were chosen given limited abundance of this rare species (Appendix: Table A1). Soil was collected at a depth of 0– 20 cm and at a distance of 0–2 m away from these adult trees in April 2011 and then sieved to eliminate any seeds and stones. Soil samples from the same species were mixed thoroughly. To separate the effects of soil microorganisms from that of potential abiotic factors, we filled 3-L pots with an identical steam-pasteurized 3:1 sandfield soil mixture. We added a small amount of live soil inoculum (10%) collected from one of the four target species to each pot. This technique has been used to dilute the potential variation that arises from abiotic factors in plant-soil feedback experiments (Mangan et al. 2010b). We planted a single germinated seedling of each tree species (low-density treatment) into half the pots containing their own live inoculum and four seedlings (high-density treatment) into the other pots. One week after the transfer of germinated seedlings into pots, the seedlings that were dead were removed and replaced with new seedlings. For each tree species, we replicated the lowdensity and high-density treatments twelve times, respectively. To determine the effect of v www.esajournals.org

Statistical analysis The field and shade-house experiments were statistically analyzed using a generalized linear 3


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mixed model (GLMM) yij ; binomialðp0 ij Þ

1 p ij A ¼ ½b0 þ b1 density logitðpij Þ ¼ log@ fixed:part 1 pij

þ½cspecies density þ lspecies þ lblock þ ðþlsite Þrandompart where yij was the binary response (alive or dead) for seedling i in block j in the shade-house experiment (or site j in the field experiment), and pij was the predicted survival probability for each seedling. The first set of brackets includes the fixed portion of the model, where b0 and b1 denotes fixed intercept and fixed slope, respectively. b1 represents the mean coefficient value of the density variable across all species, i.e., log odds ratio. The second set of brackets includes the random portion of the model, where cspecies denotes the random slope term for each species (i.e., variation among species in the coefficient of the density), lspecies characterizes the variation among species, and lblock and lsite refer to blockspecific and site-specific random intercepts, respectively, which were used to characterize the survival autocorrelation within the same block (in the shade-house) and research site (in the field). Mixed models with crossed random effects were fitted by the glmer function of the ‘‘lme4’’ package with Laplace’s method (Baayen et al. 2008, Bates et al. 2012). The fixed effects were tested by Wald Z tests and the significance of random effects were assayed by likelihood ratio tests (Bolker et al. 2009). Odds ratios (ratio of seedling survival to mortality of high density treatment vs. low density treatment) were chosen to express the effects of the density treatment on seedling survival. Odds ratio is the most common expression for the effect of independent variables on the binary response. In this study, it means the decreased possibility of survival/ mortality when increasing 3 seedlings for each species. In the GLMM model framework, the parameter b1 denotes the log odds ratio. If the log odds ratio , 0 (95% confidence interval does not overlap with 0), it would indicate negative effects of increasing density on seedling survival, and if the log odds ratio was not significantly different from 0, it would indicate no effects of increasing density on seedling survival. Finally, we used odds ratio regression to determine whether the v www.esajournals.org

Fig. 1. Density effects of four species with increasing abundance in the control treatment (a) and in the sterilization treatment (b) in the shade-house experiment. The circles are the estimated means, the thin lines are the 95% credible intervals, and the thick lines are the standard errors. The density effect was expressed as the ratio of seedling survival to the mortality in the high density treatment vs. the low density treatment (log odds ratio). The density effect , 0 (95% confidence interval does not overlap 0) indicates negative effects of increasing density on seedling survival, and the density effects not significantly different from 0 indicate no effects.

effects of density treatments on seedling survival of different species were significantly correlated with species abundance (Qian et al. 2010). All analyses were performed in R 2.15.1 (R Core Team 2014).

RESULTS In shade-house experiment, we found strong evidence for negative density-dependent effects, based on seedling survival, across all four species in the control (no sterilization) treatments (z ¼ 2.445, p ¼ 0.0145), and each of the four species that were investigated produced significant results (Fig. 1a). Furthermore, the strength of the density effect was significantly correlated with the relative abundance or the basal area of the adult trees found on the 6 ha plot (Fig. 2a). In sterilization treatment, two species (Cf and Cc) suffered stronger negative density dependence while for the other two species (Og and Bm) the overlapping confidence intervals indicated no 4


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Fig. 2. Density effect in control treatment (a) and sterilization treatment (b) as a function of abundance of adult trees in the 6 ha plots. The density effect was expressed as the ratio of seedling survival to the mortality of the high density treatment vs. the low density treatment (log odds ratio). The circles are the estimated means, and the bars indicate standard errors.

sterilization effects (Fig. 1b), suggesting that soil biota lessened negative density effect. Sterilization significantly changed seedling survival, particularly for species Cf with declined survival rate (Fig. 3). The relationship between abundance and density effect disappeared after sterilization (Fig. 2b), which suggested that soil biota were the main cause underlying this relationship. We repeated this analysis using the basal area of adult trees, a proxy for biomass, as an alternative measure of tree abundance (Comita et al. 2010) and obtained similar results (Appendix: Fig. A3). Similarly, in the field experiment, seedling density had a significant influence on survival in the control (no fungicide) treatments (z ¼ 2.453, p ¼ 0.0142), particularly for relatively rare species (Fig. 4a), and the magnitude of the density dependence was significantly correlated to species abundance (Fig. 5a). Furthermore, fungicide treatment substantially altered the density effect, with three of the four species no longer retaining significance (Figs. 4b and 6). The density effect did not correlate with abundance after the fungicide treatment (Fig. 5b), which indicated that soil pathogens were the major cause of the relationship between density and abundance. We repeated this analysis using the basal area of adult trees, as an alternative measure of tree abundance, and obtained similar results (Appendix: Fig. A4).

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DISCUSSION Both the shade-house and the manipulative field experiments clearly indicated that the more abundant tree species exhibited weaker conspecific negative density dependence and the relationship between species abundance and CNDD disappeared when the soil was treated with fungicide or was sterilized. These results indicated that soil biota were crucial to the positive relationship between CNDD and tree species abundance (Comita et al. 2010, Lewis 2010, Mangan et al. 2010b, Johnson et al. 2012). Our study suggests that the filtering effect of local CNDD on relative species abundance may be an important mechanism behind the maintenance of plant species diversity across ecosystems that range from temperate grasslands to subtropical and tropical forests (Klironomos 2002, Mangan et al. 2010b, Johnson et al. 2012). CNDD has previously been assumed to occur more strongly in abundant tree species (Connell et al. 1984, Webb and Peart 1999, Queenborough et al. 2007). However, the variations in abundance may also be a consequence of CNDD, which suggests that density dependence plays a local filtering role when shaping species abundance. Specifically, species suffering from strong CNDD may have fewer chances to establish, potentially limiting their relative abundance, while species that experience weak CNDD could establish in the proximity of conspecifics, thus 5


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Fig. 3. Seedlings survival rate of five tree species after 5 months in the sterilization and control treatment in the shade-house experiment. Abbreviations of species are as follows: Cf, Castanopsis fabri; Cc, Cryptocarya concinna; Og, Ormosia glaberrima; Bm, Bridelia monoica. Seedlings from different species were planted into pots with soil material obtained from beneath adult conspecific trees. High temperature sterilization method was used in the sterilization treatment.

allowing them to increase their relative abundance. We experimentally tested the relationship between the strength of CNDD and tree relative abundance and found that species exhibiting strong CNDD had a lower abundance in their community in a subtropical forest. Our findings are consistent with results from the tropical forest Forest Dynamics Plot (Comita et al. 2010, Mangan et al. 2010b) and from the United States across a gradient from boreal to subtropical forests (Johnson et al. 2012). Our study also indicated that soil biota were possibly a source of CNDD that was corrected with tree species abundance (Mangan et al. 2010b, Chisholm and Muller-Landau 2011, Yenni et al. 2012). However, we also noticed that there were several studies that failed to draw similar conclusions (Reinhart 2012, Reinhart et al. 2012a, b). Opposite results occurred both at the temperate forest (Johnson et al. 2012, Reinhart et al. 2012a, b) and temperature grasslands (Klironomos 2002, Reinhart 2012) seemingly indicated that the association of CNE and tree abundance was not a general process and soil biota were not able to serve as the general mechanism underlying the abundance pattern of plant community. Nevertheless, this inconsistent result may be due in part to different measures used to represent the negative effects of soil biota (Brinkman et al. 2010). The effect of plant-soil feedback was usually designed to characterize the negative effect of soil biota using shade-house condition-

Fig. 4. Density effects of four species with increasing abundance in the control treatment (a) and in the fungicide treatment (b) in the field experiment. The circles are the estimated means, the thin lines are the 95% credible intervals, and the thick lines are the standard errors. The density effect was expressed as the ratio of seedling survival to mortality of the high density treatment vs. the low density treatment (log odds ratio). The density effect , 0 (95% confidence interval does not overlap 0) indicates negative effects of increasing density on seedling survival, and the density effect not significantly different from 0 indicates no effects of increasing density on seedling survival.


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Fig. 5. Density effects in the control treatment (a) and the fungicide treatment (b) as a function of abundance of adult trees in the 6 ha plot. The density effect was expressed as the ratio of seedling survival to mortality in the high density treatment vs. the low density treatment (log odds ratio). The circles are the estimated means, and the bars indicate standard errors.

ing experiment and in grassland (Bever 1994, Klironomos 2002, Reinhart 2012) and occasionally using tree seedlings and in forest (Mangan et al. 2010b, McCarthy-Neumann and Ibanez 2013). Mangan et al. (2010b), using net pair-feedback method (Bever 2003), calculated the specific soil biota effect and successful linked it to the tropical forest community structure. While Klironomos (2002), using ‘‘home-away’’ method, obtaining similar conclusion in the grassland, Reinhart et al. (2012a, b) rejected the relationship between plant rarity and home-way soil feedback effects. Distance-dependence driven by soil biota in the context of the Janzen-Connell was inherently

consistent with the plant-soil feedback (Bever et al. 2010), whereas the effects of density dependence were used to represent the negative effect of conspecific density (Harms et al. 2000, Packer and Clay 2000, Bell et al. 2006, Comita et al. 2010, Johnson et al. 2012). Moreover, unlike the plantsoil feedback, density dependence may be attributed to resource competition rather than soil organisms. In our study, we aimed to verify whether the effect of increased seedling density on seedling survival probably turned into the abundance pattern of adult tree, as proposed by two forest demographic analyses (Comita et al. 2010, Johnson et al. 2012) and whether soil biota

Fig. 6. Seedlings survival rate of five tree species after 5 months in the fungicide and control treatment in the field experiment. Abbreviations of species are as follows: Ef, Engelhardia fenzelii; Cf, Castanopsis fabri; Cc, Cryptocarya concinna; Bm, Bridelia monoica. Seedlings from different species were directly planted into plots beneath adult conspecific trees and half of these plots were sprayed with fungicide.


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were the main contributor to this relationship between density effect and tree rarity in subtropical forest. The connection between local species-specific biotic interactions and species abundance patterns indicates that local ecological processes involving small seedlings may determine the community structure. In studies based on the Janzen-Connell hypothesis, an important and unresolved issue is whether the density dependence acting on seedlings is strong enough to determine the composition of mature trees (Freckleton and Lewis 2006). Although significant density dependence, driven by soil pathogens, is observed during the seedling stage, this effect may not translate into the maintenance of diversity in mature trees if other processes acting in later phases of the life cycle override the density dependence acting on seedlings. On the contrary, several recent studies that omitted other potential processes underling community composition directly tested the relationship between the local interactions involving seedlings and the abundance pattern of mature trees (Comita et al. 2010, Mangan et al. 2010b, Johnson et al. 2012). In line with these studies, we experimentally verified that CNDD, driven mainly by soil biota, was able to play an important role in the abundance pattern of mature trees seen in a subtropical forest. Since the ‘‘unseen majority’’ of soil organisms may have complicated interactions with each other, we should not arbitrarily rule out other potential contributors. Mycorrhizal fungi (MF) have also been shown to influence plant biodiversity and productivity (Van der Heijden et al. 1998). We observed that the change in the relationship after sterilization (elimination of soil biota) was mainly due to the increased strength of common species CNDD in the shade-house experiment (Fig. 2b), whereas in the field, the change that occurred after fungicide treatment (the specific elimination of soil pathogens) was mainly due to the decreased strength of CNDD in rare species (Fig.5b). Increasing CNDD after eliminating soil biota was opposite to the prediction that soil pathogens had played a crucial role. If soil pathogens were the main cause, we would expect eliminated or declined CNDD after sterilization (Packer and Clay 2000, Bell et al. 2006 ). v www.esajournals.org

Combined with the declined survival of species Cf and Og after sterilization (Fig. 3), these result indicated the potential role of MF and their possible functional specificity (Mangan et al. 2010a). In contrast, in the field fungicide application increased seedling survival and decreased CNDD, manifesting the important role of soil pathogens, particularly for rare species Bm (Fig. 6). Different performance of Bm in both experiments indicated that although soil pathogens decreased survival, yet sterilization also eliminated the positive effect of MF and thus did not significantly enhance seedling survival. For species Cf, when soil pathogens did not affect its seedling survival, sterilization eliminated the positive effect of MF and thus decreased the survival. Furthermore, sterilization or fungicide treatment may change the activity of other soil organisms, such as bacteria and nematodes and the interactions between them and soil-borne pathogens/MF. Taken together, we suggest that the complex interaction of soil organisms and plants influenced the seedling survival and density effects in our study. One question commonly asked is, How do rare species persist in communities if they suffer severer CNE than common species? Several recent theoretical and empirical studies have attempted to answer this question (Chisholm and Muller-Landau 2011, Kobe and Vriesendorp 2011, Yenni et al. 2012). It seems that rare species can persist even though they are subjected to stronger CNDD than common species. In our experiments, while just five species were used in consideration of the availability of seeds and germination of seedlings, paralleled shade-house and field experiments obtaining similar results should make us more confident. Nevertheless, there seems to be a pseudoreplication issue by bulking soils from different adults. While the identity of the adult has been shown to be important (Reinhart and Clay 2009), our results may over inflate the importance of strong negative soil biota at one adult tree out of the four sampled around, although we were aimed at the effects of treatments at the community level and did not attempt to clarify the variation of adults. Again, accompanying the shade-house experiment, the field experiment with tree replicates lowered the possibility 8


XU ET AL. Blundell, A. G., and D. R. Peart. 1998. Distancedependence in herbivory and foliar condition for juvenile Shorea trees in Bornean dipterocarp rain forest. Oecologia 117:151–160. Bolker, B. M., M. E. Brooks, C. J. Clark, S. W. Geange, J. R. Poulsen, M. H. H. Stevens, and J.-S. S. White. 2009. Generalized linear mixed models: a practical guide for ecology and evolution. Trends in Ecology and Evolution 24:127–135. Bradley, D. J., G. S. Gilbert, and J. Martiny. 2008. Pathogens promote plant diversity through a compensatory response. Ecology Letters 11:461– 469. Brinkman, E. P., W. H. Van der Putten, E. J. Bakker, and K. Verhoeven. 2010. Plant–soil feedback: experimental approaches, statistical analyses and ecological interpretations. Journal of Ecology 98:1063– 1073. Carson, W. P., T. A. Jill, G. L. Egbert, and S. A. Schnitzer. 2008. Challenges associated with testing and falsifying the Janzen-Connell hypothesis, a review and critique. Pages 210–241 in W. P. Carson and A. S. Stefan, editors. Tropical forest community ecology. Wiley-Blackwell, West Sussex, UK. Chen, L., X. Mi, L. S. Comita, L. Zhang, H. Ren, and K. Ma. 2010. Community-level consequences of density dependence and habitat association in a subtropical broad-leaved forest. Ecology Letters 13:695–704. Chisholm, R. A., and H. C. Muller-Landau. 2011. A theoretical model linking interspecific variation in density dependence to species abundances. Theoretical Ecology 4:241–253. Comita, L. S., H. C. Muller-Landau, S. Aguilar, and S. P. Hubbell. 2010. Asymmetric density dependence shapes species abundances in a tropical tree community. Science 329:330–332. Comita, L. S., S. A. Queenborough, S. J. Murphy, J. L. Eck, K. Xu, M. Krishnadas, N. Beckman, and Y. Zhu. 2014. Testing predictions of the Janzen– Connell hypothesis: a meta-analysis of experimental evidence for distance-and density-dependent seed and seedling survival. Journal of Ecology 102:845–856. Connell, J. H. 1971. On the role of natural enemies in preventing competitive exclusion in some marine animals and in rain forest trees. Pages 298–312 in P. J. D. Boer and G. Gradwell. Dynamics of populations. Centre for Agricultural Publishing and Documentation, Wageningen, The Netherlands. Connell, J. H., J. G. Tracey, and L. J. Webb. 1984. Compensatory recruitment, growth, and mortality as factors maintaining rain forest tree diversity. Ecological Monographs 54:141–164. Del-Val, E., and J. J. Armesto. 2009. Seedling mortality and herbivory damage in subtropical and temper-

of artifact. Based on our results, we suggest that soil organisms were important contributor to the maintenance of tree community structure. Further analysis will be required to distinguish the relative role of soil-pathogens and other soil organisms in driving this relationship. Surveys and experiments are also required to test the variations in strength and the direction of density dependence across latitudinal and altitudinal gradients to obtain more information on region-specific species diversity of forest communities.

ACKNOWLEDGMENTS We are grateful to Weinan Ye, Yi Zheng, Zhiming Zhang, Xubing Liu, Minxia Liang and Jie Li for their help in the field. This research was funded by the National Natural Science Foundation of China (grant number 31230013 and 31170398) and the ZhangHongda Science Foundation at Sun Yat-sen University.

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SUPPLEMENTAL MATERIAL ECOLOGICAL ARCHIVES The Appendix is available online: http://dx.doi.org/10.1890/ES15-00144.1.sm


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