R eports. The effect of environmental and phylogenetic drivers on community assembly in an alpine meadow community
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1 Ecology, 93(11), 2012, pp Ó 2012 by the Ecological Society of America The effect of environmental and phylogenetic drivers on community assembly in an alpine meadow community ZHONGLING YANG, 1,2 JEFF R. POWELL, 3 CHUNHUI ZHANG, 1 AND GUOZHEN DU 1,4 1 Key Laboratory of Arid and Grassland Ecology under Ministry of Education, Lanzhou University, Lanzhou China 2 Life Science College, Xinxiang University, Xinxiang China 3 Hawkesbury Institute for the Environment, University of Western Sydney, Richmond, NSW 2753 Australia Abstract. To predict the consequences of environmental change on plant communities at local scales, one needs to understand the regional drivers structuring these communities. Here, we used a formal analytical framework incorporating functional traits and evolutionary histories to understand the importance of environmental filtering and species interactions in the assembly of alpine plant communities. The study was conducted in the Tibetan Plateau using field plots experiencing changes in land use (fertilization and grazing). We observed evidence for both trait-based convergence (associated with plant height and tissue nitrogen) and divergence (associated with specific leaf area) within alpine plant communities, suggesting that environmental filtering and limiting similarity are acting simultaneously during assembly processes. Although we did not observe evidence of phylogenetic niche conservatism in relation to intensified land use, we did observe support for the phylogenetic structure of plant communities influencing community-weighted mean trait values, suggesting that evolutionary constraints represent a significant driver of community assembly in this system. Therefore, evolutionary and ecological processes may have independent effects on alpine plant communities facing land use intensification. Key words: alpine meadow; environmental filtering; evolutionary history; fertilization; functional redundancy; grazing; limiting similarity; niche conservatism; phylogenetic signal; Tibetan Plateau; trait conservatism; trait convergence. INTRODUCTION To predict the consequences of land use change on the structure and composition of communities at local scales, it is necessary to understand the regional drivers underlying the structuring of these communities. In general terms, communities assemble following deterministic processes, associated with environmental filtering and biotic interactions (Keddy 1992, Cornwell and Ackerly 2009), and stochastic processes, associated with environmental disturbance and demographic dynamics within local and regional species pools (Hubbell 2001, Dornelas et al. 2006). Multiple processes can act simultaneously (Cornwell and Ackerly 2009, Pillar et al. 2009). For example, processes linked to species niches can drive assembly processes in opposite directions: species that occur together in communities and experience similar environmental conditions are likely to share phenotypic traits because of environmental filtering (Keddy 1992, Weiher et al. 1998) whereas, at the same time, competitive exclusion is likely to limit the similarity of species that persist in these environments (MacArthur and Levins 1967). Therefore, communitylevel patterns in trait convergence and divergence can Manuscript received 10 December 2011; revised 4 June 2012; accepted 5 June 2012; final version received 29 June Corresponding Editor: D. C. Laughlin. 4 Corresponding author. guozdu@lzu.edu.cn 2321 determine the importance of these constraints during community assembly (Pillar et al. 2009) and help to predict how assembly processes may respond to changes in local environments and regional species pools. Phenotypic trait values are not randomly distributed among species, but tend to covary based on the degree of phylogenetic relatedness among species, with extended periods of shared ancestry resulting in similar phenotypic traits (trait conservatism) and ecological similarities (niche conservatism) among species (Darwin 1859, Wiens and Graham 2005). A growing literature has demonstrated broad patterns of trait conservatism (e.g., Ackerly 2004, Cavender-Bares et al. 2006). Therefore, it is important to incorporate phylogenetic information into analyses of trait-based assembly processes along environmental gradients to adequately evaluate the interplay between phylogenetic and ecological trait convergence (Silvertown et al. 2006, Duarte 2011). In addition, because the composition of regional species pools is largely determined by historical factors related to biogeographical and macroevolutionary processes, these factors will probably influence the ability of plant communities to respond to environmental changes (Crisp et al. 2009). Alpine meadows are among the most impacted ecosystems currently facing the selection pressures due to changes in climate and land use (Klein et al. 2007). In the present study, we adopt the general analytical
2 2322 ZHONGLING YANG ET AL. Ecology, Vol. 93, No. 11 framework proposed by Pillar et al. (2009) and Pillar and Duarte (2010) for detecting assembly patterns associated with trait divergence (TDAP) and trait convergence (TCAP) in an alpine grassland, and linking these patterns to evolutionary relationships in the metacommunity and to environmental change associated with intensified land use. Specifically, we ask the following three questions: 1) Is there evidence for trait-based community assembly patterns in alpine meadow ecosystems? 2) To what extent does environmental change influence plant community composition via effects on traitbased community assembly patterns? 3) Does phylogenetic niche conservatism constrain alpine meadow plant community responses to environmental change? METHODS Study site The study was carried out on a broad, flat site at 3500 m above sea level at the Lanzhou University research station of alpine meadow and wetland ecosystems. The station is located at Maqu ( N, E), Gansu, China, in the eastern Tibetan plateau (see Plate 1). Mean annual temperature is 1.28C, ranging from 108C in January to 11.78C in July. Mean annual precipitation over the previous 35 years has been 620 mm, mainly distributed during the short, cool summer. The area has 2580 h of sunshine and more than 270 days/yr of frost (Luo et al. 2006). Mean aboveground biomass is g/m 2 (dry mass). There are, on average, vascular plant species per 0.25 m 2. The vegetation is dominated by clonal Kobresia graminifolia, Poa botryoides, Elymus nutans, Anemone rivularis, and others. In October 1999, a field site measuring m, located in a flat area (slope,18) was fenced. Experimental design We used a split-plot design with two fertilization levels (unfertilized [0] and fertilized at a rate of 30 g/m 2 [30]) nested within two grazing treatments (grazed [G, no enclosure], ungrazed [E, with enclosure]), resulting in four land use treatments (E 0,E 30,G 0, and G 30 ). We established 32 permanent m plots on 30 May 2007, with 16 plots placed within a fenced enclosure. For both the grazed and ungrazed treatments, the plots were arranged in a regular four by four matrix, with 2-m buffer strips between plots. Outside of the enclosure, vegetation was moderately grazed by ungulates, with 110 yaks (0.18/ha) and 2200 sheep (3.68/ha) during all months except for 40 days between the end of July and mid-september when the animals were moved to higherelevation pastures. The enclosure excluded grazers from mid-april to the end of November of each year. We acknowledge the nonindependence of individual plots within the enclosed and grazed treatments. Previous observations suggest that spatial heterogeneity in plant community richness and composition at the site is unlikely to act as a confounding factor, particularly for the plot sizes used here; however, interpretations related to these treatments should still be treated with caution. The nutrient gradient was established using slow-release ammonium phosphate pellets [(NH 4 ) 2 HPO 4, Tianjin International Trading Company, Tianjin, China] at the rate of 0 and 6.3 g/m 2 of nitrogen and 0 and 7.0 g/m 2 of phosphorus, respectively. The fertilizer was applied in May each year during a rain event. Vegetation monitoring In 2009, we sampled one m quadrat within each plot in early September, when biomass had reached its peak (Luo et al. 2006). The quadrats were at least 0.5 m from the edge of the plot to avoid marginal effect. In each plot, species richness, percent cover, species biomass, and species height (three heights of each species) were recorded. Mean abundance was calculated in terms of the species biomass of eight replicate quadrats in each treatment. We made sure to limit this number to species that actually rooted within the quadrat, rather than counting also species with parts overhanging the plot. Species compositional responses to the treatments are not our main focus and are presented in the Appendix. Trait measurement We sampled the species that appeared in the process of vegetation monitoring as much as possible. Finally, we chose 48 common species in G 0,46inG 30,47inE 0, and 42 in E 30 (provided in Table A1 of the Appendix), which accounted for.95% of the aboveground biomass in these communities. Only aboveground parts were sampled at fruiting time from 20 July to 5 September in 2008 and 2009, due to the difficulties in collecting entire roots in an alpine meadow. In each treatment, we randomly sampled 20 individuals of each species and then measured the individual height; in total, 3660 individuals were investigated each year. For clonal plants, we treated a ramet as an individual (Luo et al. 2006). Each individual was dried in an oven at 808C to constant mass and then weighed using a Sartorius balance accurate to 10 4 g (Sartorius TEN , Hong Kong Labware, Hong Kong, China). To measure the species specific leaf area (SLA), we randomly sampled 20 whole leaves of each species in each treatment during the year in 2008 and The fresh leaves were scanned to measure leaf area using the software ImageJ v (Rasband 2008). They were dried at 808C to constant mass, and were weighed using a Sartorius balance accurate to 10 4 g. Tissue nitrogen [(nitrogen concentration (mg/g) of aboveground parts] is measured by digestion with concentrated H 2 SO 4 and 30% H 2 O 2 and colorimetric analysis using a Lachat Autoanalyzer BS63-A8 (Alpkem, College Station, Texas, USA) for total N (EPA Method A) with three replicates in each treatment for each species during
3 November 2012 COMMUNITY ASSEMBLY PATTERNS 2323 the year for 2008 and Seeds were collected at the start of natural dispersal in Enveloped seeds were spread on tables and allowed to air-dry to a constant mass at room temperature (;158C) before being weighed. Mean seed mass of each species was determined by weighing three replicates of 100 seeds. Estimates of community-weighted means for each trait under the land use treatments are presented in the Appendix. Data analysis We searched for independent patterns of trait divergence assembly patterns (TDAP) and trait convergence assembly patterns (TCAP), as a function of land use and phylogenetic trait and niche conservatism, using the general analytical approach described in detail by Pillar et al. (2009) and Pillar and Duarte (2010). Briefly, this was done by estimating the degree of correlation among matrices containing species abundances in local communities, experimental treatments applied to these communities, distributions of traits (based on the mean trait values for each species across the experimental treatments), and relative measures of shared evolutionary history. The plant phylogeny was generated using phylomatic (Webb and Donoghue 2005) in association with the R version of the Angiosperm Phylogeny Group III supertree (available online). 5 Branch lengths from Wikstrom et al. (2001) were incorporated into the tree and undated nodes were estimated using the bladj algorithm in phylocom (Webb et al. 2008). Evidence of environmental filtering (TCAP E ) was indicated by a significant correlation between community distances based on environmental characteristics (D E ) and those based on community-weighted mean trait values (D T ). Evidence of limiting similarity (TDAP E ) was indicated by a significant correlation between D E and community distances based on species compositions after fuzzy weighting by trait similarities (to generate degrees of belonging of species to groups based on shared traits; D X ) and removing the effect of D T ; this evidence is derived from patterns observed in the metacommunity and limiting similarity may be restricted to only some communities along the studied ecological gradient (Pillar and Duarte 2010). Evidence of phylogenetic signal at the metacommunity level related to trait convergence (PSM TCAP ) was indicated by a significant correlation between D T and community distances based on phylogenetic structure (species compositions after fuzzy weighting by phylogenetic similarities; D P ), whereas that related to trait divergence (PSM TDAP ) was indicated by a significant correlation between D P and D X after removing the effect of D T. When appropriate, we tested whether trait-based assembly patterns along the environmental gradient were 5 mediated by shared evolutionary histories (phylogenetic niche conservatism) using Shipley s d-separation approach (as in Pillar and Duarte 2010); we compared two models in which trait distributions within communities (T) corresponds to (1) environmental characteristics (E) indirectly via community phylogenetic structure (P) (E! P! T) or (2) each of these matrices independently (P! T E), and determined whether each model provided an adequate fit to the data. To test the significance of the estimated correlations, we compared these against null models derived by permutation of the input matrices; random matrix T was generated by permuting among species in the species 3 trait matrix (B), random matrix X by permuting among species fuzzy sets in matrix U (defining sets based on trait similarities), and random matrix P by permuting among species fuzzy sets in matrix Q (defining sets based on phylogenetic similarities). More detail can be found in Pillar et al. (2009) and Pillar and Duarte (2010). P values were based on permutation tests employing 999 randomizations. All analyses were performed in R v (R Development Core Team 2011) using the SYNCSA package v.1.2 (Vanderlei 2011). We highlight significant (P, 0.05) and marginally significant (P, 0.1) responses in the text. RESULTS In general, evidence for trait convergence and trait divergence was dependent on the traits included in the analysis. In relation to environmental variation, there was no evidence of trait convergence or trait divergence when all traits were considered (Table 1). However, as in the null model approach, tissue nitrogen (q ¼ 0.38, P ¼ ) and plant height (q ¼ 0.37, P ¼ ) each showed moderate evidence of trait convergence within communities along the environmental gradient (environmental filtering), whereas SLA (q ¼ 0.28, P ¼ ) showed moderate evidence of trait divergence within communities along the environmental gradient (limiting similarity). In relation to the phylogenetic structure of communities, there was moderate evidence of trait convergence within communities when all traits were considered (q ¼ 0.63, P ¼ ), and stronger evidence when considering tissue nitrogen (q ¼ 0.85, P ¼ ), SLA (q ¼ 0.76, P ¼ ), or plant height (q ¼ 0.87, P ¼ ). Phylogenetic structure was also observed within communities in relation to trait divergence when all traits were considered (q ¼ 0.90, P ¼ ). However, this signal was not captured by any of the individual traits (Table 2). There was no evidence of either plant biomass or seed mass contributing to trait convergence or trait divergence, either in relation to the environmental variation or community phylogenetic structure (Table 1). Different traits exhibited different phylogenetic patterns. Tissue nitrogen, SLA, and plant height were significantly correlated with the phylogenetic matrix,
4 2324 ZHONGLING YANG ET AL. Ecology, Vol. 93, No. 11 Trait-based assembly patterns associated with trait divergence (TDAP) and trait convergence (TCAP) in the station of alpine meadow and wetland ecosystems of Lanzhou University, Lanzhou, China. TABLE 1. Trait 3 environment correlations Trait 3 phylogeny correlations Environmental filtering Limiting similarity Environmental filtering Limiting similarity Traits q P q P q P q P All plots All traits Tissue nitrogen SLA Plant biomass Seed mass Plant height Enclosed plots All traits Tissue nitrogen SLA Plant biomass Seed mass Plant height Grazed plots All traits Tissue nitrogen SLA Plant biomass Seed mass Plant height Notes: Shown are correlations (q) of the trait-based patterns with evolutionary relationships in the metacommunity and with environmental change associated with intensified land use. Environmental filtering suggests that species occurring together share phenotypic traits because they experience similar environmental conditions. In limiting similarity, competitive exclusion is likely to limit the similarity of coexisting species (i.e., there is limit of species niche overlap). Boldface type indicates significant correlations with P, SLA is specific leaf area. TABLE 2. Phylogenetic signal in traits at the metacommunity levels [q(pt)], with boldface indicating significant correlations at P, Phylogeny by environment correlations Phylogenetic signal in trait P and E independently influence T E affects T indirectly via P Traits q(pt) P q(pe) P q(te.p) P All plots Tissue nitrogen SLA Plant biomass NA NA Seed mass NA NA Plant height Enclosed plots Tissue nitrogen SLA NA NA Plant biomass NA NA Seed mass NA NA Plant height Grazed plots Tissue nitrogen NA NA SLA NA NA Plant biomass NA NA Seed mass NA NA Plant height NA NA Notes: In the latter two groups of columns, we tested two alternative path models for causal relationships between trait distributions within communities (T), environmental characteristics (E), and community phylogenetic structure (P) in an alpine grassland, with the strongest support attributed to the path models with nonsignificant P values. Although both path models were supported when the analysis included all plots, the analysis of enclosed plots supports the hypothesis that land use change and the phylogenetic structure of the community independently influence trait-based assembly [q(pe)] over the hypothesis of phylogenetic niche conservatism related to land use change [q(te.p)].
5 November 2012 COMMUNITY ASSEMBLY PATTERNS 2325 FIG. 1. Biplots of the first two principal-components axes associated with analyses of (A) species traits, (B) community-weighted mean trait values (based on matrix T), and (C) phylogenetic patterns within communities (based on matrix P) in alpine plant communities. Numbers in panel (A) correspond to the species labels in Fig. A2 of the Appendix); species are ranked based on the order that they appear in the plant phylogeny so that neighboring values are more likely to co-occur within clades. Trait names in panels (A) and (B) reflect the scores associated with these traits in the analyses. In panels (B) and (C), solid circles represent enclosed plots, and open circles represent grazed plots; fertilized and unfertilized plots are indicated by black and gray circles, respectively. Values in parentheses in the axis labels indicate the proportion of inertia accounted for by the first two constrained axes. whereas plant biomass and seed mass were not, regardless of whether the enclosed vs. grazed treatments were analyzed together or separately (Table 2). Because tissue nitrogen and plant height (in the analysis of the full data set and when restricted to the enclosed plots) and SLA (only in the full data set) all contributed to patterns in community assembly in relation to environmental gradients and phylogenetic structure, we used these traits to test the hypothesis that phylogenetic niche conservatism was driving assembly patterns along our experimental environmental gradients. For the full data set and for each of the traits, neither hypothesis was rejected, suggesting that both hypotheses have support. However, we had reason to believe that plant community responses to the fertilization treatment differed among the enclosed and grazed plots, hindering meaningful interpretation: fertilized and unfertilized communities diverged with respect to plant traits (Fig. 1B), phylogenetic structure (Fig. 1C), and species composition (Appendix) within the enclosure,
6 Reports 2326 ZHONGLING YANG ET AL. Ecology, Vol. 93, No. 11 PLATE 1. The study site and surrounding scenery (Walaka, Maqu [ N, E], Gansu, China, in the eastern Tibetan plateau). Clockwise from upper left: local scape of the study site, our colleagues in the field, view of the Yellow River, and the Yellow River on a foggy morning. Photo credits: Z. Yang. but not under the grazing treatment. Indeed, when restricting the analysis to the enclosed plots, the hypothesis related to phylogenetic niche conservatism received less support than the alternative hypothesis that trait-mediated community assembly was driven independently by the environmental gradients and phylogenetic structure (Table 2). We did not perform this analysis on the grazed plots because we did not observe any correlation between the traits and the fertilization treatment in these plots (Table 1). DISCUSSION Effect of land use on trait-based community assembly Here we have explicitly shown that assembly processes in alpine plant communities have both local and regional drivers. With respect to local drivers associated with land use, previous studies have shown that fertilization and grazing have strong effects on the composition and structure of alpine plant communities (Niu et al. 2010, Yang et al. 2011), although others have demonstrated that these effects may be conditional on other changes in the environment (Klein et al. 2007). Our data suggest that fertilization may affect these dynamic processes by influencing the distributions of traits associated with plant height and nitrogen uptake; assembly processes are influenced by the matching of these traits to environmental conditions generated by land use change. In addition, we found moderate evidence for fertilization affecting interspecific interactions among plant species, driving divergence within communities with respect to traits related to SLA. Finally, our data suggest that grazing reduces the importance of these traits with regard to matching local fertility levels. This latter result may be due to estimated plant height being less variable among species and less responsive to fertilization under grazing pressure. Increased plant height is often related to competitive ability, and the prevalence of this trait within plant communities is often observed to increase following fertilization (e.g., Niu et al. 2010). Small-statured plants, on the other hand, have been reported to be favored by grazing (e.g., Diaz et al. 2007); although we did not observe convergence with regard to this trait in grazed communities, any constraint on plant height appeared to be released in the unfertilized enclosures. Grazing in low-fertility grasslands generally creates conditions of
7 November 2012 COMMUNITY ASSEMBLY PATTERNS 2327 higher availability of light and nutrients, so species with fast acquisition of resources (high SLA and tissue nitrogen) tend to be favored (Grime 2001), although these traits did not appear to drive convergence in the grazed communities studied here (Tables 1 and 2). However, we did observe evidence that fertilization in the absence of grazing resulted in species that were less apt to produce nitrogen-rich tissue (possibly suggesting relatively poor rates of nutrient acquisition) becoming more abundant. Trait-based community assembly patterns at regional scales In general, trait-based assembly processes within communities were also linked to the evolutionary histories among community members, with evidence of phylogenetic convergence patterns (clustering) with respect to traits that showed evidence of phylogenetic conservatism (tissue N, SLA, and plant height), but not those traits that were randomly distributed among clades (plant biomass and seed mass). These patterns were also observed to be more visible in the enclosed plots, whereas they tended to disappear outside of the enclosure. Within these communities, phylogenetic divergence patterns (overdispersion) were also observed with traits under study within the enclosed plots, although this was not captured by any of the traits individually, possibly as a result of the pattern being driven by different traits in different communities. Phylogenetic divergence patterns can result from either biotic interactions, such as competition, causing overdispersion of conserved traits, or environmental filtering on ecologically important traits with independent convergent evolution in different clades (Schluter 2001). No evidence for phylogenetic niche conservatism in relation to land use intensification Our study suggested that trait-based community assembly in the studied alpine plant communities is dependent on changing land use as well as phylogenetic constraints on trait distributions. Using the experimental treatments associated with land use, we did not observe phylogenetic niche conservatism, with respect to community responses to herbivory and fertilization, to be a likely driver of assembly processes in these communities. This model of assembly was less well supported than one in which phylogenetic signal in traits and land use factors acted independently on assembly. Although phylogenetic niche conservatism may constrain traits that limit the distributions of species along environmental gradients (Cavender-Bares and Wilczek 2003, Wiens and Graham 2005), we did not observe that to be the case in this alpine grassland, at least with regard to the studied traits. Because we did not find evidence for phylogenetic niche conservatism, it is possible that the impacts of land use on alpine plant communities may be predicted largely based on the distribution of traits within the metacommunity; however, we recommend that additional alpine systems be studied to confirm this result. That said, phylogenetic relationships among plant species were clearly an important driver of trait-based assembly processes, particularly in the absence of grazing, suggesting that some aspect of the environment independent of the experimental treatments may provide a hint of phylogenetic niche conservatism. If the environmental tolerances of traits and species are phylogenetically conserved, then differences in the environment could act as a filter, and closely related traits and species would be more likely to coexist. However, as we observed, this also creates the potential for biotic interactions driving divergence in these and/or other traits, further altering the composition of communities. CONCLUSIONS A large number of studies have analyzed the phylogenetic structure of communities to examine the evidence for neutral or niche-based processes in community assembly. These have challenged the assumption that evolutionary processes are not relevant to community assembly, and begin to provide predictive information about the responses of communities and traits to environment variation (Cavender-Bares et al. 2009) and inform niche modeling exercises (Willis et al. 2010). Based on the general analytical framework proposed by Pillar et al. (2009) and Pillar and Duarte (2010), we found that traits with significant phylogenetic signal at the metacommunity level exhibited environmental filtering, which could indicate species phylogenetic niche conservatism in relation to specific environmental conditions (Ackerly 2004, Cavender-Bares et al. 2006). We have demonstrated this to be the case for alpine plant communities, with responses dependent on trait-based assembly patterns linked to the phylogenetic structure of the metacommunity, but independently of intensification of land use, which also influenced community assembly. Additional systems will need to be studied to determine whether predictions about species and ecosystem response to changes in land use and other forms of environmental change (e.g., climate) may be better informed by incorporating the shared evolutionary history of relevant functional traits at regional scales. ACKNOWLEDGMENTS Zhongling Yang and Jeff R. Powell contributed to this paper equally. We thank Hui Guo, Shujun Wen, Xin Chen, Peng Jia, Wei Li, Liujie Wang, Xiao Yang, Wenxiang Hu, Junyong Li, and many others at the Maqu Rangeland Workgroup for assistance in both the field and lab. We also thank Valério Pillar and an anonymous reviewer for helpful comments on an earlier version of the manuscript. This project was supported by Key Program of National Natural Science Foundation of China (Grant No: ).
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