Jintun Zhang?Bin Zhang?Zhiying Qian

Functional diversity of Cercidiphyllum japonicum,communities in the Shennongjia Reserve,central China

Jintun Zhang?Bin Zhang?Zhiying Qian

Functional diversity is significant to ecological processes of plantcommunities.We analyzed the variation of functional diversity of endangered species,Cercidiphyllum japonicum,communities along an elevational gradient in the Shennongjia Reserve,central China.Sixty plots of 10 9 20 m from 1,350 to 2,050 m were setup and species composition,traits and environmental variables were measured and recorded.These data were analyzed using five functional diversity indices,functional attribute diversity,modified functionalattribute diversity,plotbased functional diversity,community based functional diversity and Rao’s functional diversity indices(Rao’s index), Functional diversities of C.japonicum communities were rich and varied greatly.Functionaldiversity declined nonlinearly with increasing elevation.Functionaldiversity was significantly correlated with species richness and heterogeneity.Elevation was a key environmental variable influencing functional diversity and species diversity.The five functional diversity indices were all effective for measuring functional diversity of communities.Functional diversity can be used as an indicator of conservation efficiency of endangered species such as C.japonicum.

Endangered speciesFunctional traitFunctional diversityEnvironmentalgradientConservation

Introduction

Functional diversity refers to the diversity of functional composition of ecological communities and is often represented in one of two general ways,either as indices of individual traits or by combining information from multiple traits to generate one or severalcomposite indices,and hence is also called functional trait diversity(FTD)(Petchey and Gaston 2006;Ville′ger et al.2008;Zhang et al. 2012a).It has been proposed as a fundamental concept in the description of ecological process and ecosystem function,and itstresses differences between species in terms of their functions in communities(Tilman etal.2001;Petchey and Gaston 2002).Functional diversity may relate to the breadth of environmental conditions that are suitable for species within a community and can also be related to the strength ofhabitatfilters(Cornwelletal.2006).Therefore, functional diversity may be related to the conservation of endangered species and their survival in communities (Song and Zhang 2013).

The variation of functional diversity can be linked to ecological gradients.Elevational gradient is known to be a decisive factor shaping the spatial patterns of vegetation and species diversity in mountainous areas(Zhang 2011). The pattern of change in species diversity along elevation gradients has frequently been tested in ecology.The most commonly observed pattern is that maximum diversity is found at intermediate elevations(Austrheim 2002;Zhang etal.2013).However,the pattern of variation in functional diversity along elevational gradients is not clear and needsadditionalstudy(Mason etal.2005;Butterfield and Suding 2013).

Cercidiphyllum japonicum Sieb.Et Zucc.(Cercidiphyllaceae)is a deciduous tree species and was listed as one of national protected plants at the second category in China (Guan 1979).Itis mainly distributed in subtropicalmountainous regions,such as Hubei,Sichuan,Hunan,and Guizhou provincesin China,and the Shennongjia region isone of itsdistribution centersin China.C.japonicum haseconomic value as spice,medicine,and timber,and has been listed as an endangered species due to its dioecism,low setting rate, low survivalrate of seedlings and other biologicalfeatures, and due to human exploitation(Liu 2009).C.japonicum communities generally occur on both sides of valleys or mountain streams.Themaintenanceofbiologicaldiversity is important for conservation of C.japonicum and its communities.Previous research on C.japonicum focused on its geographic distribution,breeding,medicinal chemistry, seedling establishmentin naturalcommunities,and threatsto its survivalin the wild(Zhang etal.2006;Liu 2009;Fu etal. 2012).However,the functional diversity of C.japonicum communities has notbeen studied.In the presentstudy,we assessed the pattern ofvariation in functionaldiversity of C. japonicum communities along an elevational gradient in Shennongjia National Nature Reserve.We tested the hypothesis thatthe highestfunctionaldiversity was atmid elevations and identified the key environmental variable influencing plant functional diversity.We analyzed the relationships between functionaldiversity and conservation of this endangered species.

Materials and methods

Study area

Shennongjia National Nature Reserve is located at 109590–ll0580E,3l150–3l570N in western Hubei Province,central China(Fig.1).Elevation ranges from 500 to 3105.4 m a.s.l.and most peaks of the Shennongjia range are above 1,500 m as1.High elevation,deep ravines,and steep slopes characterize the physiognomy of the Shennongjia range.This area is deeply affected by a southeast subtropical monsoon with abundant precipitation and a moderate mean temperature.

Fig.1 Geographical location of Shennongjia National Nature Reserve,Hubei Province,P.R.China

The annual mean temperature decreases with altitude, from approximately 13.8C at460 m to 7.4C at1,700 m and the mean monthly temperature is over 25C in summer,while the mean monthly temperature is lower than -4C in winter.Annual mean precipitation is 1219.93 mm,ranging from 800 to 2,500 mm and increasing with elevation.Most rain falls from May to October. Soils in Shennongjia Reserve also change with elevation, from red-yellow soil,mountain yellow soil,mountain yellow-brown soil,mountain brown soil,mountain dark brown meadow soilto mountain gray-dark brown soilfrom the lowest to highest elevations.The vegetation changes along the elevation gradient:evergreen broadleaved forest under 900 m,mixed evergreen and deciduous broadleaved forest between 900 and 1,500 m,deciduous broadleaved forest between l,500 and 2,000 m,mixed conifer and deciduous broadleaved forestbetween 2,000 and 2,600 m, and subalpine conifer forest and subalpine shrubs and meadows over 2,600 m(Zhang et al.2005).

Sampling

According to the distribution of C.japonicum communities,60 plots of 10 m 9 20 m were sampled along the elevational gradient between 1,350 and 2,050 m a.s.l. Species name,cover,height,basal area and individual abundance for tree species,and name,individual or tussock abundance,cover and height for shrubs and herbs were recorded in each plot(Zhang 2011).The plant height was measured by using a height-meter for trees and a ruler for shrubs and herbs.The basal diameter of trees was measured by using a caliper and was used to calculate basal area.A total of 138 plant species were recorded in 60 plots.Fourteen functional traits were selected to illustrate plant species function in communities(Table 1).Photosynthesis pathway,seed dispersal, pollination manner,root system and nitrogen-fixing were identified from local flora.Life-form,leaf form,leaf hair, plant height,flowering date,flowering period,fruit maturation date,fruit maturation period and life cycle were observed and measured in the field.To calculate functional diversity,a data matrix of functional traits 9 species was constructed for each sample plot,and,in total, there were 60 data matrices for 60 plots.

Table 1 Plant functional traits and their values in Cercidiphyllum japonicum communities in Shennongjia National Nature Reserve,Hubei Province,central China

Elevation,slope,aspect and litter thickness were also recorded for each plot.The elevation at each plot was measured by using a GPS,the slope and slope aspect were measured by using a compass meter,and litter thickness was measured by using a ruler(Zhang 2011).Elevation, slope and litter thickness were reading values,while the aspect measurements were classified from 1 to 8 in the following way:1(337.6–22.5),2(22.6–67.5),3 (292.6–337.5),4(67.6–112.5),5(247.6–292.5),6 (112.6–157.5),7(202.6–247.5),and 8(157.6–202.5). Higher aspect category values corresponded to greater sunlight availability.

Data analysis

We used the following 5 indices to calculate functional diversity:

Functional attribute diversity(FAD)

FADaimed at estimating the dispersion of species in trait space as the sum of the pairwise species functional distances(Walker et al.1999):

where,dijis the functional distance between species i and j in functional trait space.

Modified FAD(MFAD)

For a given set of data of for S species and N traits,the functional species were defined.The set of functional species resulted from combining the species with the same values in allthe traits into only one functionalspecies.The number of entities in the data matrix will was be reduced from S to M(M B S),and,accordingly,the pairwise distances were reduced from an S 9 S to an M 9 M matrix. MFADwas calculated as:

where,dijis the distance between functional units‘i’and‘j’,and M is the number of functionalunits.

Functionaldiversity based on dendrogram(FDp and FDc)

A Functional diversity index based on a dendrogram is the totalbranch length ofthe functionaldendrogram thatcan be constructed from information aboutspecies functionaltraits (Petchey and Gaston 2006).There were two choices:FDp isa plotbased index which recalculates the dendrogram foreach plot,butin doing so the desirable property of‘setmonotonicity’doesnothold.FDc isa community based index which correctsforthe lack ofmonotonicity thatariseswhen there is a particularunique dendrogram foreach plot.

Rao’s index(FD)

Rao’s index indicates expresses the expectation of trait dissimilarity between two randomly chosen individuals in a community(Rao 1982).

Fig.2 Change(polynomialregressions)offunctionaldiversity along an elevational gradient in Cercidiphyllum japonicum communities in Shennongjia National Nature Reserve,HubeiProvince,centralChina. FAD,MFAD,FDp,FDc and Rao refer to functional attribute diversity,modified functionalattribute diversity,plotbased functional diversity,community based functionaldiversity and Rao’s functional diversity indices,respectively

where,dijis the functionaldistance between species i and j, piand pjare the relative abundances of species i and species j,and S the totalnumber of species in the community.

Species diversity

Three species diversity indices,one for species richness (species number S),one for species heterogeneity(Shannon-Wiener index H0),and one for species evenness(Pielou index E),were used to calculate species diversity values(Pielou 1975).

Shannon-Wiener heterogeneity index:

Pielou evenness index:

where,Piis the relative abundance of species i,and S the number of species recorded in a plot.

Spearman correlations were used to analyze relationships of functional diversity,environmental variables and species diversity.Polynomial regression was used to test the variation pattern of functional diversity along the elevational gradient.These were analyzed by SPSS(version 16.1).

Results

The functional diversity was rich in C.japonicum communities at Shennongjia Reserve and all the functional diversity values varied greatly(Fig.2).FAD varied from 6.0 to 24.0,MFAD from 1.16 to 5.57,FDp from 22.31 to 90.71,FDc from 23.00 to 95.86,and Rao’s index from 7.97 to 16.54.All five indices showed the same pattern of change where the functional diversity decreased gradually with increasing elevation from 1,350 to 2,050 m(Fig.2). Their relations were non-linear(best fitted)and this suggested that elevation was a significant factor to functional diversity in communities.These functional diversity indices showed the same pattern because they were significantly correlated with each other(Table 2).Among the fiveindices,FAD,MFAD,FDp and FDc were more significantly correlated with each other than with Rao’s index (Table 2).Except for elevation,other environmental variables such as slope,aspect and litter thickness did not significantly influence spatial patterns of functional diversity,and only litter thickness was significantly correlated with FDp(Table 3).

Table 2 Spearman correlation coefficients between functional diversity indices for Cercidiphyllum japonicum communities in Shennongjia National Nature Reserve of Hubei Province,central China

Table 3 Spearman correlation coefficients between functional diversity indices and environmental variables for Cercidiphyllum japonicum communities in Shennongjia National Nature Reserve of Hubei Province,central China

Functional diversity was significantly correlated with species diversity in C.japonicum communities,i.e.four of the five indices,FAD,MFAD,FDp and FDc,were significantly correlated with species richness and species heterogeneity(Shannon-Weiner index),and Rao’s index was correlated with species heterogeneity(Table 4). Functional diversity and species richness showed a positively non-linear relation,i.e.functional diversity gradually increased with the increase of species richness (Fig.3).The relationships of functional diversity with species evenness in communities were not significant (Table 4).The correlations of species diversity with environmental variables were similar to those of functional diversity with environmental variables,i.e.elevation significantly influenced species richness and species heterogeneity(Table 5).

Table 4 Spearman correlation coefficients between functional diversity and species diversity for Cercidiphyllum japonicum communities in Shennongjia National Nature Reserve of Hubei Province, central China

Discussion

Functional diversity can be used to quantify relationships between species composition,community structure,function and environment in communities(Mason et al.2005; Zhang etal.2012a).Functionaldiversity varied greatly in C.japonicum communities in Shennongjia Reserve,which suggested that C.japonicum communities differed in species diversity,structure,function and inner environment. Functionaldiversity was closely related to elevation,which was consistent with the conclusion that elevation was the key environmental variable affecting community structure, diversity and distribution in this reserve(Zhang etal.2005, 2006).All five functional diversity indices showed the same pattern wherein functionaldiversity of C.japonicum communities decreased in a polynomial way along the elevational gradient(De Bello et al.2006;Zhang et al. 2013).Maximum functional diversity was recorded at 1350 m and minimum functional diversity was recorded at 1,850–1,900 m.C.japonicum communities usually occurred in mountain valleys and along rivers and water conditions were good in the communities(Liu 2009).The change of functional diversity was mainly influenced bythe temperature gradient(Zhang et al.2006).In Shennongjia Reserve,the subtropical climate zone was below 800 m,the warm temperate zone was at800–1,500 m,the temperate zone was at 1,500–1,900 m,the cold-temperate zone was at 1,900–2,500 m and the cold zone was above 2,500 m(Zhang et al.2005).The decline in functional diversity with increasing elevation from 1,350 to 2,050 m followed the climate change from warm temperate to temperate and to cold temperate,and hence followed the decrease of temperature(Yuan et al.2012).Temperature was therefore a limiting factor affecting the distribution, structure and composition of C.japonicum communities and further affecting their functional diversity in Shennongjia Reserve(Zhang 2011).

Fig.3 Relationships(polynomialregressions)of functionaldiversity with species richness in Cercidiphyllum japonicum communities in Shennongjia NationalNature Reserve,HubeiProvince,centralChina. FAD,MFAD,FDp,FDc and Rao refer to functional attribute diversity,modified functionalattribute diversity,plotbased functional diversity,community based functionaldiversity and Rao’s functional diversity indices,respectively

Table 5 Spearman correlation coefficients between species diversity and environmental variables for Cercidiphyllum japonicum communities in Shennongjia National Nature Reserve of Hubei Province, central China

Besides elevation,litter thickness had some effecton the change of functional diversity in C.japonicum communities,while slope and aspect had no significant effects on functional diversity patterns.This was because these variables did notvary widely across the localdistribution range of C.japonicum communities(Zhang et al.2005).

Functional diversity was significantly correlated with species richness and heterogeneity in C.japonicum communities in Shennongjia Reserve.Functional diversity showed a polynomial increase with species richness,i.e. their relationships were non-linear(Song and Zhang 2013). This suggests thatfunctionaldiversity and species richness were interrelated but different(Mason et al.2005;Zhang et al.2013).There are some variations in functional traits that might go beyond the variation that can be explained only by taxonomic variation(Ricotta and Moretti 2008). Both functional diversity and species diversity can be used as indicators of community composition,structure,function and environment,while one cannot replace the other (de Bello et al.2009;Zhang et al.2013;Casanoves et al. 2011).Therefore,functional diversity can be used as a conservation indicator for endangered species such as C.japonicum and their communities(Zhang et al.2013; Butterfield and Suding 2013).

The five methods used to quantify functional diversity were allsuccessfulin describing the quantity and variation of functional diversity in C.japonicum communities in Shennongjia Reserve,which suggests that these indices were all effective in the analysis of functional diversity in these plantcommunities(Mason etal.2005;De Bello etal. 2009;Zhang etal.2013).These indices were all based on the functional distances between species and were theoretically similar(Casanoves et al.2011).The indices used were all significantly correlated with each other,which further suggested thatthese methods provide similar results in the analysis offunctionaldiversity in plantcommunities (Diaz etal.2007;Zhang etal.2012b).

Regression analysis between functional diversity and importance value of C.japonicum in communities showed a non-significant negative relation(nearly significant,no presentation here),and this trend suggested thatfunctional diversity should be maintained within a specified range for effective conservation of C.japonicum.Functional diversity can be used to indicate efficiency of conservation management in nature reserves.

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31 August 2013/Accepted:19 February 2014/Published online:8 January 2015

Project funding:The study was financially supported by the National Natural Science Foundation of China(Grant No:31170494)and the Specialized Research Fund for the Doctoral Program of Higher Education(Grant No.20120003110024).

The online version is available athttp://www.springerlink.com

Corresponding editor:Zhu Hong

College of Life Sciences,Beijing Normal University, Xinjiekouwai Street 19,Beijing 100875, People’s Republic of China

e-mail:Zhangjt@bnu.edu.cn